Dissociation between seeing and acting: Insights from common marmosets (Callithrix jacchus)

Behavioural Processes 89 (2012) 52–60

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Dissociation between seeing and acting: Insights from common marmosets (Callithrix jacchus) Trix Cacchione a,∗ , Judith Maria Burkart b a b

Department of Psychology, Cognitive and Developmental Psychology, University of Zurich, Binzmühlestrasse 14/21, CH-8050 Zurich, Switzerland Anthropological Institute & Museum, University of Zurich, Switzerland

a r t i c l e

i n f o

Article history: Received 9 May 2011 Received in revised form 10 October 2011 Accepted 21 October 2011 Keywords: Continuity Dissociation Gravity bias Inhibitory control Solidity

a b s t r a c t Perception-based measures often reveal much earlier competencies than action-based approaches. We explored this phenomenon generally labeled as “knowledge dissociation” in 28 common marmoset monkeys (Callithrix jacchus) using a paradigm where subjects had to localize a food item dropped down an opaque tube. Experiments 1 and 2 assessed common marmoset monkeys’ gravity bias in an action based version of the tubes task. Experiments 3 and 4 investigated whether marmosets’ performance increases in an action-free task context where they simply look at objects falling down a tube. The results suggest that common marmosets have some intuition of continuity/solidity constraints when tested with perception based measures even though these principles do not appear to guide their search for falling objects. © 2011 Elsevier B.V. All rights reserved.

1. Introduction The developmental research of past decades often reveals dissociations between what human infants and non-human primates know as revealed by action and as revealed by perception. This is especially true for developmental trajectories found with action versus perception based investigations in the core domain of object continuity/solidity (e.g., Baillargeon, 2002; Baillargeon et al., 1995; Berthier et al., 2000; Hespos and Baillargeon, 2001; Hood et al., 2000a, 2003; Kim and Spelke, 1992; Spelke et al., 1992). In the present study we focus on a knowledge dissociation that was observed with the widely studied tubes task. When tested with this task, human children and various other mammal species showed the so-called “gravity bias”, a prominent example of a perseverative response bias (Cacchione and Call, 2010; Cacchione et al., 2009; Hood, 1995, 1998; Hood et al., 2006; Tomonaga et al., 2007). In many instances researchers found that human infants and other mammal species expected dropped objects to fall straight down. Even when a solid obstacle (the tube) impeded a straight vertical fall, they robustly searched at the location specified by the gravitational line. This finding is in strict contrast with perception based evidence that knowledge about continuity/solidity is very early traced in human infants and in at least two non-human primate species (e.g., Hespos and Baillargeon, 2001; Santos and Hauser, 2002; Santos et al., 2006; Spelke et al., 1992). In the present study

∗ Corresponding author. Tel.: +41 44 635 7498; fax: +41 44 635 7489. E-mail address: [email protected] (T. Cacchione). 0376-6357/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2011.10.010

we tested common marmosets (Callithrix jacchus) with two versions of tubes task (a standard action version and perception-based version) with the aim to contribute to a better understanding of this striking pattern of knowledge dissociation. In the following, we first briefly sketch research on the tubes task, then summarize contrasting evidence found with perception based methodologies and finally specify the rationale for the present experiments. 1.1. Gravity biased search When confronted with a vertically falling object, human children, non-human primates, and dogs search for the object directly below the release point (Cacchione et al., 2009; Cacchione and Call, 2010; Hood, 1995, 1998; Hood et al., 1999; Osthaus et al., 2003). This behavior is generally interpreted as conveying the expectation that all unsupported objects fall in a straight vertical line. In his seminal work, Hood (1995) identified the gravity error in children younger than 3 years of age. He presented 2–4-year-old children with an invisible displacement task where the goal was to locate a ball that was dropped down one of three intertwined opaque tubes connected to one of three hiding places. Search errors of 2- and 2.5-year-olds occurred significantly more often at the hiding place directly underneath the release place. Hood (1995, 1998) interpreted this behavior as stemming from an underlying naïve theory of gravity because the error was not observed when upward or horizontal motion was presented (Hood, 1998; Hood et al., 2000b). He suggested that children develop a sensitivity for gravity by detecting statistical regularities in the myriad of gravity events that they witness in their everyday lives. This sensitivity leads to specific

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expectations about the behavior of dropped objects and eventually culminates in a perseverative bias. He further proposed that 3-yearolds overcome the bias not due to a theory change but because they acquire the ability to inhibit unwarranted gravity responses (Freeman et al., 2004; Hood et al., 2006). Hood’s explanation for the bias as generated by naïve reasoning was generalized to instances of gravity biased search in non-human animals (Hood et al., 1999). The most pronounced tendency for gravity responses has been reported in cotton-top tamarins (Saguinus oedipus) when tested with the tubes task outlined above (Hood et al., 1999). Despite extensive training and cost incentives for correct choices (only one choice was allowed), tamarins continued selecting the wrong box, i.e. the one in the direction of gravity. These results strengthened the impression that monkeys are more affected by inhibitory failures than human children, because children do not show gravity biases in this task (Hood et al., 2000a). Because these studies were run on adult monkeys, the authors concluded that they (like children) are guided by a naïve gravity theory but that in contrast to children, monkeys never acquire sufficient inhibitory control to suppress the bias (see Gómez, 2005 for a review). In contrast to monkeys, great apes (Cacchione et al., 2009; Cacchione and Call, 2010) and dogs (Osthaus et al., 2003) eventually overcome repetitive gravity responses (which might in case of apes be partly due to their greater inhibitory abilities, e.g., Amici et al., 2008; Deaner et al., 2006; Rumbaugh and Pate, 1984). 1.2. Solidity/continuity constraints in perception The finding that in a search context expectations about gravity override knowledge of object continuity/solidity is very remarkable because these principles are thought to be part of an innate cognitive core shared by primate (and probably also other mammal) species (Spelke, 1994; Spelke et al., 1992; Spelke and Kinzler, 2007). Generally, perception-based methods reveal much earlier competences than action-based investigations. This contrast was attributed to the fact that object knowledge proceeds infants’ capacity to act on objects (Spelke, 1994). Developmental psychologists provided various explanations for infants’ initial limitation in executive functions such as their problems to inhibit response biases (Diamond, 1991), their problems with the planning of means-end sequences (Baillargeon et al., 1990; Hood and Willats, 1986; Keen, 2003) and their inability to form representations that support action (Munakata et al., 1997). However, even 2-year-old toddlers (an age where the executive problems associated with direct action are no longer decisive) were found to be unable to act on continuity/solidity knowledge, that is, on principles whose violation 2–4-month-old infants perceptively detect (Ahmed and Ruffman, 1998; Berthier et al., 2000; Hood, 1995; Hood et al., 2000a,b, 2003). As a consequence the use of perception-based measures (such as habituation–dishabituation and violation of expectancy tasks) has been criticized (Baillargeon, 2004; Bogartz et al., 2000; Cashon and Cohen, 2000; Haith, 1998; Hood, 2001; Munakata, 2000; Rivera et al., 1999; Schilling, 2000). Particularly controversial was the issue of what kind of knowledge systems are tapped by perception-based measures, and of whether explicit conceptual knowledge can actually be demonstrated by perception-based measures. Cases of action/perception dissociations are not exclusive to human cognition but were equally observed in non-human primates in tasks involving gravity/solidity constraints (Cacchione and Krist, 2004; Hood et al., 2000a,b; Santos and Hauser, 2002; Santos et al., 2006; Spelke et al., 1992; Leslie, 1994). To clarify why action and perception tasks often give contrasting evidence recent comparative research focused on knowledge dissociations themselves comparing responses of different species in action- and

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perception-based versions of the same task type (Santos and Hauser, 2002; Santos et al., 2006). Santos and Hauser (2002) tested whether rhesus macaques would detect solidity violations when looking at invisible displacements without being engaged in active search. Participants saw a food object being dropped behind an occluder on a solid table-like apparatus. The removal of the occluder revealed one of two possible outcomes: a consistent outcome where the object was positioned on top of the shelf (consistent with the principle of solidity), or an inconsistent outcome where the object was positioned below the shelf (inconsistent with the principle of solidity). Rhesus macaques looked reliably longer when the object appeared to travel through the solid shelf, suggesting that they have some sensitivity for solidity constraints. Thus, the findings were in sharp contrast with what was observed in the action version of the task (where they neglected solidity and searched below the shelf). 1.3. The present studies The current study sets out to investigate the continuity/solidity dissociation in common marmosets in the context of the original tubes task (Hood, 1995). As Santos and colleagues, we used exactly the same task to compare both response modes (action and perception). The tubes task is even better suited to investigate knowledge dissociations because (a) response biases are reported to be highly robust in this task, and (b) a dropped object that “apparently” travelled to the gravity location violates both continuity and solidity constraints. To our knowledge, this is the first adaptation for looking time measures of the tubes task. Further, adding a new primate species offers important insights from a comparative perspective on the dissociation phenomenon. Data on multiple species (more distantly as well as more closely related to humans) are required to be able to make strong inferences about the distribution and evolution of cognitive abilities. Moreover, to compare common marmosets with the closely related cotton top tamarins might be especially promising given that gravity biased search is proposed to be directly linked to a lower inhibitory control and marmosets were found to outperform tamarins in some tasks that require inhibitory control (Stevens et al., 2005). In the present studies we assessed gravity bias in common marmoset monkeys’ and compared their performance in action-based (Experiment 1 + 2) and perception-based methodology (Experiment 3 + 4). To make sure that prior experience with one of the two task types does not influence reactions two sub samples were tested in a between-subject design. In Experiments 1 and 2, we confronted marmosets with two variations of the original tubes task (Hood, 1995) and compared their performance to that of other mammal species tested with the same action-based methodology. In Experiments 3 and 4 we investigated whether marmosets are more likely to exhibit adequate intuitions when tested in an action-free task context (perception-based measures) where executive demands are expected to be less influential. 2. Experiment 1: Gravity bias in common marmosets? The goal of the first experiment was to assess gravity biased search in common marmosets and compare their performance to that of other mammal species tested. To achieve ideal comparability we presented common marmosets with the tubes task originally introduced by Hood with human infants and later used to test great apes, dogs and monkeys. 2.1. Method Participants. Participants were 7 adult common marmosets (C. jacchus), a small New World monkey species, housed at the Primate

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Fig. 1. Tubes apparatus with three boxes used in Experiment 1.

Station of the Anthropological Institute of the University of Zurich. All individuals were born in captivity, 5 were reared by their family, and 2 hand-reared for the first 5 weeks but then reintroduced to their respective families. During experimentation, they were housed in outdoor cages that were equipped with branches, ropes, and different sitting places and covered with natural soil. There were 3 adult males and 4 adult females, aged between 1 year 4 months and 7 years 3 month (average = 4 years 3 months, SD = 28.8 months). Five animals formerly participated in experiments exploring social dynamics in the context of reproduction but had never been subjected to any cognitive task. Apparatus. The apparatus (Fig. 1) used in the action task was a scaled down remake of the original apparatus of Hood (1995). It consisted of a grey plastic frame with three chimneys of 3.5 cm diameter separated by 6.5 cm on the upper section. The lower section (20 cm below) contained three goal boxes (4.5 cm × 4.5 cm × 4.5 cm). All goal boxes had a hole on the top and a front door. A single plastic opaque tube connected the upper and the lower section. Marmosets were lured into a transparent Plexiglas box (30 cm × 30 cm × 45 cm) that was placed at the front door of the home cage. The front of the box was made of wire mesh and could be covered by an opaque screen, all other sides were opaque. This setting allowed us testing the animals individually without separating them from their mates acoustically or by long distances, which reduced the stress of being isolated almost completely. Design. All animals were run on a baseline (consisting of 1–2 sessions, each with 10 trials) and a test condition (consisting of two sessions, each with 16 trials). They were tested with only one baseline or test session per day. The baseline condition served to check for potential box preferences and to ensure that all marmosets master the basic test prerequisites. In the baseline condition the tube was removed. The animals were run on 10 trials in which a food item was randomly dropped in full view of the marmosets in one of the three goal boxes. If they found the food item on first attempt in 9 out of 10 trials they were judged to have passed the baseline condition. Animals that did not reach this criterion were retested with another baseline session the next day. Animals that successfully completed the baseline condition proceeded to the test condition. Two test sessions were scheduled to assess the strength of a potential bias, and to determine whether it would decline over trials after the repeated localization of the food in the box connected to the tube. In each test session marmosets were presented with

one of two tube configurations (upper left chimney to lower right goal box or vice versa). Half of them started with an upper left/lower right configuration, the other half with the opposite tube arrangement. During the second session, the configuration was changed, so that all animals were tested with both start configurations. If they successfully located the food on first attempt in four out of five trials the tube configuration was switched to the opposite configuration. This was done to test if correct search can be generalized to a new location or if marmosets go on searching the food in the previously enforced box. The first trial after the configuration switch was assessed as a generalization trial. Across both test sessions, each time a subject reached criterion (four out of five) the tube arrangement was flipped to the opposite configuration. Therefore, within one test session a subject could receive a maximum of three generalization trials (and thus a maximum of three tube configuration changes); over both test sessions it could receive a maximum of six generalization trials (and a maximum of three tube configuration changes), respectively. If search was not successful tube configuration was not changed until the 16 trials of a session were completed. Thus, marmosets that never reached criterion received no generalization trials (and thus no tube configuration changes) within test session and maximally one configuration change over both test sessions (because the starting configuration was changed from session 1 to session 2).

2.2. Procedure Pre-training. Participants were first familiarized with the tube and the apparatus in their home cages. During the initial phase marmosets were allowed to explore the tube. The experimenter held the tube in front of the animals and made them look through it. To ensure that they were aware that objects can travel through the tube, the experimenter dropped three non-food objects (pieces of bark) down the tube holding it in a vertical position. She made sure the each individual marmoset tracked the complete dropping process at least twice. After this, the apparatus without the tube was placed in the home cage for 15 min to give the participants the opportunity to examine it in detail. Baseline. The next day, the marmosets were run on the baseline condition. Each of them was lured individually in a Plexiglas box and the apparatus placed in front of it. The experimenter then opened all three boxes to demonstrate that they were empty and closed them again. The participant was allowed to open the box doors and to explore the compartments. Then the apparatus was removed out of reach of the animal (10 cm away from the wire mesh) and all box doors closed. A small food item was waved back and forth over one of the goal boxes. If the subject tracked it the food was released through the top hole into the goal box. Now, the apparatus was pushed back in reaching distance of the marmoset. They were allowed to search for the food until found. This procedure was repeated up to 10 trials. The search behavior was recorded on a check sheet. Participants that met criterion (9 out of 10) proceeded to the test condition. Test. Each participant was presented with two sessions on 2 consecutive days, immediately following the baseline condition. Participants were again placed in the Plexiglas box and the apparatus positioned in front of them. To prevent that the marmosets located the food relying on acoustic cues, white noise was played. The experimenter attached an opaque tube from the upper left chimney to the lower right goal box (or vice versa). A food item was moved back and forth over the chimney with the tube attached. If the participant tracked the food it was dropped. Then the apparatus was moved in reaching distance and the marmosets were allowed to search for the food until found. The order of the boxes searched was recorded.

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Session Fig. 4. Percentage of correct and incorrect responses for all 16 trials in both sessions in Experiment 1 comparing successful and unsuccessful subjects. *Successful subjects (reaching criterion 3–4 times, n = 4); **unsuccessful subjects (reaching criterion 0–2 times, n = 3). Fig. 2. Frequency of each of the responses in the first trial for both sessions in Experiment 1.

2.3. Results Baseline. All except one animal passed the baseline in one session. One subject needed two sessions. First trial responses. Fig. 2 presents the proportion of each of the responses in the first trial for both sessions. None of the 7 subjects chose the correct box on first attempt in the first trial (binomial test: p < .001). However, there was no significant bias towards particular responses in the first trial of first (2 (1, N = 7) = 0.143, p = .71) or second session (2 (1, N = 7) = 2.000, p = .37). This means that subjects did neither choose the correct box nor did they show a clear gravity bias. Although four marmosets chose the correct box in the first trial of the second test session there was no significant improvement between the first and the second session in the frequency of correct first trial responses (McNemar test: p = .13, N = 7). Focusing solely on the errors collapsed across sessions, we found that subjects did not make more gravity than middle errors in the first trial responses (Wilcoxon test: z = 0.71, p = .48). Overall performance per session. Fig. 3 presents the percentage of correct, middle and gravity biased responses for all the trials (not just the first trial) in both sessions. There was a significant reduction in the percentage of gravity errors (Wilcoxon test: z = 1.992, p < .05) but no significant improvement in the percentage of correct responses from session 1 to 2 (Wilcoxon test: z = 1.521, p = .13). However, comparing performance between the first eight trials of session 1 and the last eight trials of session 2 revealed a significant improvement in correct responses (Wilcoxon test: z = 2.201, p < .05). Focusing solely on the percentage of errors revealed that 80

marmosets made reliably more gravity than middle errors in the first session (Wilcoxon test: z = 2.032, p < .05). This difference disappeared in the second session (Wilcoxon test: z = .211, p = .83). Generalization. Fifty-seven percentage of the marmosets reached criterion (four out of five correct) at least once in the first session, and 86% of them at least once in both sessions. Some of the marmosets reached criterion up to 4 times during both test session whereas others never reached it (individual differences are further addressed below). Recall that each time a subject reached criterion it was presented with the opposite tube arrangement to check if it would go on selecting the previously reinforced box or if it would switch to the new correct location (generalization trials). In the first generalization trial, marmosets neither preferred the correct (binomial test: p = .35) nor the gravity biased location (binomial test: p = .32, with three selecting the gravity, two the middle and one the correct box). Over all generalization trials, however, they preferred the correct box (binomial test: p < .05). This preference was present already in the second generalization trial (binomial test: p < .05). Individual differences. An examination of the performances on an individual level reveals important inter-individual differences. While some marmosets easily reached criterion up to 4 times (6 times would be the maximum across both sessions), others never reached it. Fig. 4 compares the percent of each of the responses of successful marmosets (reaching criterion 3–4 times, n = 4) and unsuccessful marmosets (reaching criterion 0–2 times, n = 3) in both sessions. In contrast to the rest of the sample the unsuccessful marmosets did not improve across sessions. Rather, there was a reduction of correct responses and an increase of middle responses in this group. The possible sources of these differences are further addressed in the result section of Experiment 2. 2.4. Discussion

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Session Fig. 3. Percentage of correct and incorrect responses for all 16 trials in both sessions in Experiment 1.

Common marmosets did not show a reliable gravity bias in Experiment 1. Not even in the first trial of the first test session did they significantly prefer the gravity box. However, they apparently tended to search for the object in proximity of the release point since all marmosets selected either the gravity or the middle container on their first attempt and erroneous searches were more often directed to the gravity than to the middle container in the first test session. But the tendency to search in the gravity area was certainly less pronounced than in cotton-top tamarins that were found to show a high rate of gravity biases (Hood et al., 1999). For example, 57% of the marmosets reached criterion (four out of five correct) at least once in the first session, and 86% of them at least once in both sessions. This is remarkable in comparison to the tamarins in the Hood et al. (1999) study who reached this criterion more rarely,

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22% in session 1 and 56% in session 2. Instead, as dogs (Osthaus et al., 2003) and great apes (Cacchione and Call, 2010; Cacchione et al., 2009), common marmosets appeared to behave more flexibly in this task. Remarkably and rather unexpectedly, in contrast to dogs, the marmosets adopted strategies more elaborate than simple location learning, as some of them even learned to locate the object after a tube configuration change in the generalization trials. There were substantial inter-individual differences in performance. While a group of “successful” individuals quickly learned to localize the object and to generalize this behavior to a new tube configuration, the performance of the “unsuccessful” ones even deteriorated. This suggests that besides between-species variation, there also exists considerable individual within-species variation. However, even the unsuccessful marmosets did not – as could be derived from an inhibition account – resort to gravity biases. Instead they developed the strategy to select the middle container, a strategy that was also observed in tamarins and in dogs, but not in human children and great apes. 3. Experiment 2: Does performance improve when middle strategy is barred? Some marmosets developed the strategy to select the middle container. This strategy was not observed in children and great apes, but in dogs and cotton-top tamarins and might reflect the bias’ rootedness in the experience of gravity events. According to Hood et al. (1999) the strategy to select the middle container reflects the bias’ rootedness in the experience of gravity events and appears because participants fail to differentiate between gravity and middle box and prefer both to the correct box which is less likely to be the landing location of an object that travels straight down. Thus, they suggest that search would almost exclusively be directed at the gravity box, if the middle box is not available. In contrast to this prediction, Osthaus et al. (2003) found that dogs learned to search the correct location even more quickly if the middle container was not available. The present experiment investigated how marmosets’ performance is affected if the middle container is removed. 3.1. Method Participants. As in Experiment 1 participants were 7 adult common marmosets (C. jacchus), housed at the Primate Station of the Anthropological Institute of the University of Zurich. All individuals were born in captivity, and all of them were family-reared. There were 2 adult males and 5 adult females, aged between 1 years 7 months and 6 years 6 month (average = 3 years 7 months, SD = 24.64 months). All of them formerly participated in experiments exploring social dynamics in the context of reproduction but had never been subjected to any cognitive task. None of them had participated in Experiment 1. Apparatus. The apparatus was similar to that used in Experiment 1 with the following exceptions: only two chimneys were on the upper section (4 cm diameter), separated by 9 cm. They were connected to only two goal boxes (4.5 cm × 5.5 cm × 6.0 cm) on the lower section (the middle box was removed). To further facilitate the differentiation of the various parts of the apparatus, it was colored: blue frame, red tube, and yellow boxes. Design and procedure. Design and procedure were the same as in Experiment 1. 3.2. Results Baseline. Three animals passed the baseline in one session. Two needed two sessions, and another 2 needed three sessions. First trial responses. Fig. 5 presents the proportion of the two possible responses in the first trial for both sessions. Two of 7

Fig. 5. Proportion of correct and gravity responses in the first trial for both sessions in Experiment 2.

marmosets chose the correct box on first attempt in the first trial (binomial test: p = .45) of the first session. There was no significant improvement between the first and the second session in the frequency of correct first trial responses (McNemar test: p = 1.00, N = 7). Overall performance per session. Fig. 6 presents the percentage of correct and gravity biased responses for all the trials (not just the first trial) in both sessions. There was only a marginally significant improvement of correct responses from session 1 to 2 (Wilcoxon test: z = 1.897, p = .06). However, comparing performance between the first eight trials of session 1 and the last eight trials of session 2, we found a significant improvement in correct responses (Wilcoxon test: z = 2.032, p < .05). Generalization. Seventy-one percentage of the marmosets reached criterion (four out of five correct) at least once in the first session, and all of them at least once in both sessions. In contrast to Experiment 1, the majority of the marmosets reached criterion twice, all of them reaching it either once or twice (performance differences between Experiments 1 and 2 are further addressed below). Only 1 of 7 marmosets selected the correct location in the first generalization trial (binomial test: p = .13). Also, across all generalization trials, they reliably preferred the gravity box (Wilcoxon test: z = 2.449, p < .05) that is, the location where the food could be found in prior trials. Comparison between three-box and two-box versions of the task. Marmosets did not choose the gravity box more often in the first trial of the two-box than in the three-box version of the task (Fisher’s exact test, 2 (1, N = 7) = 0.311, p = .50). Analyzing potential

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Session Fig. 6. Percentage of correct and incorrect responses for all 16 trials in both sessions in Experiment 2.

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differences in the overall occurrence of correct choices or gravity errors between the two-box and the three-box version of the task we have to take care of the different chance levels. Thus we calculated for each monkey the relative number of correct choices (number of correct choices/divided by the total number of tubes/divided by the number of trials) and the relative number of gravity errors (number of gravity errors/divided by the total number of tubes/divided by the number of trials) and run them on a Mann–Whitney U test. The relative amount of correct choices between the two-box and the three-box version of the task did not differ neither in the first (Mann–Whitney U test, z = −1.674, p = .094) nor in the second test session (Mann–Whitney U test, z = −1.307, p = .191). However, marmosets made reliably more gravity errors in the two-box version than in the three-box version of the task in both the first (Mann–Whitney U test, z = −3.151, p < .01) and second test session (Mann–Whitney U test, z = −3.155, p < .01). Inter-individual differences. We further analyzed possible roots of inter-individual differences by pooling the data of Experiments 2 and 3. This revealed that individual differences were mainly connected to sex differences. Overall, females less often searched the correct location (Mann–Whitney test, z = 2.202, p < .05) and marginally more often selected the gravity location (Mann–Whitney test, z = 1.935, p = .052). Systematic age differences were not observed. 3.3. Discussion The removal of the middle box obviously influenced marmosets’ behavior in this task. Even though they still did not show a reliable preference for the gravity container, they made reliably more gravity errors in the two-box version compared to the three-box version of the task. Further, they reached criterion less often in the twobox task and tended to select the gravity box (i.e., the previously rewarded box) also in the generalization trials. This supports Hood’s thesis that middle box selection might occur because marmosets fail to differentiate between gravity and middle box. If marmosets fail to suppress a gravity response, both gravity (most likely) and middle box (second likely) are selected more often than the correct box. Thus, if the middle box is removed, gravity responses increase because middle box selections are now directed at the gravity box. This suggests first, that straight down responses are associated with gravity events (i.e., the farther a goal location deviates from the vertical falling line the less likely it is selected) and second, that marmosets may experience more difficulties in suppressing gravity responses depending on the task context. 4. Experiment 3: Gravity or correct box- which do marmosets preferably look at? The present experiment confronted marmosets with a looking time version of the same task to test if they have any expectations about where a dropped object moved after it disappeared out of view. Even though marmosets were not able to spontaneously locate a dropped object in an action context, they still might have some intuitions regarding the objects’ location when simply looking at dropping events. 4.1. Method Participants. Participants were 7 naïve adult common marmosets (C. jacchus) housed at the Primate Station of the Anthropological Institute of the University of Zurich. They were born in captivity and all of them are family-reared. Their age ranged from 1 year 1 months to 2 years 11 months (average = 2 years 1 month, SD = 9 months). Some of the animals formerly participated

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in social learning experiments. None of them had prior experience with the search task. Apparatus. The apparatus was identical to the one used in the action task of Experiment 2. The apparatus with two goal boxes was selected for the looking time task for the following reasons. First, as revealed in Experiment 2, the middle box complicates the interpretation of the results. Second, if the middle box is present, there should also be an event in which the object is revealed in the middle box. However, a presentation of three test events is impractical for a violation of expectancy (VoE) methodology. Finally, the marmosets’ performance was more biased in the two-box version than in the three-box version. If they should show a preference for the correct location, it could not be explained by the greater simplicity of the two-box version. Marmosets were presented with two events where an object was dropped down a tube and either appeared in the box connected to it (consistent event) or in the unconnected gravity box (inconsistent event). However, the upper section of the tube was tamped to stop the dropped object. Instead the food was always placed in the respective goal box beforehand and never travelled down the tube. A mechanism allowed opening the doors simultaneously. Procedure. For the looking time version of the tubes task, we employed the so-called violation of expectancy (VoE) methodology. It is based on the assumption that infants (and non-human primates) look longer at events that violate their expectations. Because we wanted to be sure to measure pre-existing expectations, we employed the familiarization free methodology proposed by Wang et al. (2004). Again, marmosets were individually lured into the same testing box already used in prior action tests. The wire mesh front of the box was replaced by a transparent Plexiglas which enabled filming of the looking behavior of the animals in detail. An additional screen allowed interrupting visual access to the scene in front of the box. All other sides of the box were opaque. Participants first received a pre-training identical to that described above in Experiments 1 and 2 to familiarize marmosets with the apparatus. After the pre-training, all participants were presented individually with two test events, a consistent and an inconsistent one. The order of the presentation was counterbalanced across participants. Half of them first saw the consistent event; the other half was first presented with the inconsistent event. The test events were presented live by the experimenter. At the beginning of each event, the animal sat in the Plexiglas box and the apparatus was placed directly in front of it. The screen was lowered to prevent the animal from seeing the baiting of the goal box. In the consistent test event, the experimenter baited the box connected to the tube; in the inconsistent event, the gravity box was baited. Then the screen was raised. The experimenter took another food item and waved it above the chimney connected to the tube. If the participant tracked it, the food was released. If it did not track the entire releasing process, the screen was closed and opened again and the procedure repeated. In order to avoid acoustic cues, the released food item never travelled down the tube but remained invisible in the upper section of the tube which was tamped to stop the dropped object. Then both doors were opened simultaneously and the food item was either revealed in the box attached to the tube (tube box, consistent event) or in the box directly underneath the release point (gravity box, inconsistent event). Looking behavior was recorded for 10 s following the opening of the doors. At the end of the test, all marmosets got a food reward, irrespective of their performance. Coding. A camera, positioned directly behind the apparatus, recorded the experimental session. The videos were digitalized and imported in Adobe Premiere Pro. Two raters blind to the experimental condition analyzed all digitized clips frame by frame (25 frames/s). Looking times were assessed for the duration of 10 s following the opening of the doors. Looking time was coded as

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or due to the need for more time to scan events with food/tube end dissociations, respectively. To rule out these possibilities the following experiment was run as a control.

7

Looking time (sec)

6 5

5. Experiment 4: Control for intrinsic preferences and scanning time

4

gravity box tube box

3 2 1 0

Experiment 3

Experiment 4 (control)

Fig. 7. Mean looking time at the gravity box (not connected with the tube) and at the tube box (connected with the tube) in Experiments 3 (food is dropped) and 4 (control condition: involves no dropping event). *p < .05.

the amount of time a subject looked at the apparatus as a whole. Inter-rater concordance was 94.6%, inter-rater reliability K = 0.89 (Cohen’s Kappa). Statistical analysis was performed on the raw data from the first rater. 4.2. Results Fig. 7 shows the mean looking times at the congruent (tube box) and incongruent (gravity box) test events of Experiment 3. The marmosets looked longer in the impossible, inconsistent test event (M = 6.23 s; SD = 2.44 s) than in the possible, consistent test event (M = 3.42 s; SD = 2.22 s; paired-samples t-test: t(6) = 4.560, p < .01). An examination of the individual data showed that all participants looked longer in the impossible test event than in the possible test event. A 2 × 2 ANOVA with repeated measure for “type of test event” (within) and “trial order” (between) revealed a significant main effect for “type of test event” (F(1, 5) = 17.129; p < .01), but no effect for trial order (F(1, 5) = 0.062; p = .94). The interaction was not significant. Thus, the participants looked reliably longer at the inconsistent test event where the food appeared in the gravity box than in the consistent test event where the food appeared in the box that was connected to the tube, irrespective of the order of the presented events. 4.3. Discussion Marmosets looked longer when a dropped object was revealed in the unconnected box directly underneath the release point, that is, in the box specified by gravity. This suggests that they did not expect that all objects travel straight down and therefore did not anticipate the object to be revealed in the gravity box. Instead, this might suggest that at least perceptually they are sensitive to the constraints of object continuity/solidity and react to apparent violations of these core principles. This is remarkable given their performance in the actions tasks of Experiments 1 and 2 where they were often unable to locate the object, and suggests an action/perception dissociation. However, there are alternative explanations why marmosets looked longer at the impossible gravity outcome. First, they might simply have preferred to look at the event where tube end and food item were dissociated. Similarly, it is possible that longer looking time at the inconsistent event was due to the need for more time to scan events with food/tube end dissociations in order to pick up all information. It is important to make sure that the results of Experiment 3 are not simply due to a preference for events in which tube end and food item are dissociated,

In Experiment 4 we presented marmosets with exactly the same test events as in Experiment 3 with the exception that the food was never dropped. The rationale was that, if marmosets really look longer at the inconsistent event of Experiment 3 because they experience a violation of solidity, then this effect should disappear if no dropping (and consequently no solidity violation) occurs. If, on the other hand, they simply prefer to look at food/tube end dissociations, need longer scanning times to encode them or look longer at the reward in the gravity box for any other reason not related to the dropping event, then they should still look longer at the inconsistent event regardless of whether an object was dropped or not. 5.1. Method Participants. Participants were 7 naïve adult common marmosets (C. jacchus) housed at the Primate Station of the Anthropological Institute of the University of Zurich. They were born in captivity, 4 are family-reared and 3 are hand-reared for the first 5 weeks but then reintroduced to their natal families. Their age ranged from 1 year 3 months to 9 years 9 months (average = 4 years 1 month, SD = 46 months). Two of them had previously participated in social learning experiments, and 3 in tasks on perspective taking (Burkart and Heschl, 2007). None of them had prior experience with the search task. Apparatus. The apparatus was identical to the one used in Experiment 3. Procedure. The procedure was identical to Experiment 3 with the following exceptions: the experimenter never dropped a food item. Instead, she held her empty hand above the chimney connected to the tube and moved the fingers. If the participant tracked it, both doors were opened simultaneously. No violation of solidity took place. In one event, the food item was revealed in the box attached to the tube and in the other event, in the unconnected gravity box. Again, looking behavior was recorded for 10 s following the opening of the doors. At the end of the test all subject got a food reward, irrespective of their performance. Coding. Coding was done as described in Experiment 3. Inter-rater concordance was 97.0%, inter-rater reliability K = 0.94 (Cohen’s Kappa). Statistical analysis was performed on the raw data from the first rater. 5.2. Results To test if marmosets really experienced the events of Experiment 3 as being different from the control events of Experiment 4, we calculated an ANOVA with outcome (gravity vs. correct box) as within, and experiment (3 vs. 4) as between subject variable. There was a main effect for outcome (F(1, 12) = 13.99, p < .01) and a significant interaction of experiment × outcome (F(1, 12) = 7.26, p < .05). This suggests that longer looking at one outcome over the other occurred not in both experiments equally. Focusing on the performance in each experiment revealed that only marmosets in Experiment 3 looked reliably longer at the inconsistent gravity event (see Section 4.2) whereas looking times did not reliably differ between the two events in Experiment 4 (paired-samples ttest: t(6) = 0.733, p = .49). Fig. 7 shows the mean looking times of the two events of Experiment 4. On average, marmosets looked 4.74 s at the gravity test event (SD = 2.60 s) and 4.28 s at the tube test event

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(SD = 2.92 s). An examination of the individual data showed, that 3 participants looked longer at the gravity event, 3 longer at the tube event and 1 marmoset looked equally long at both events. A 2 × 2 ANOVA with repeated measure for “type of test event” (within) and “trial order” (between) yielded no significant results for “type of test event” (F(1, 5) = 0.349; p = .58) and for trial order (F(1, 5) = 0.430; p = .54). Also, the interaction was not significant. Thus, in contrast to Experiment 3 the participants of Experiment 4 did not prefer one event over the other. 5.3. Discussion Marmosets looked equally long at both test events if no food item was dropped down the tube and therefore no continuity/solidity violation occurred. In contrast to Experiment 3 where marmosets looked longer at the event where the food appeared in the gravity box, they did not have an above chance preference for one of the two events. This suggests that the longer looking at the inconsistent test event of Experiment 3 was not simply due to a baseline preference for events with food/tube end dissociations or the need to conduct longer scanning to encode them. Instead, it is possible that longer looking was associated with the violation of object continuity/solidity. Taken together, the results of Experiments 1–4 suggest that common marmosets exhibit a dissociation between performance in perception and action versions of the tubes task. Thus, marmosets appear to have adequate intuitions about the future trajectory of objects dropped down the tube when tested in an action-free task context where inhibitory problems are less influential. 6. General discussion In a looking time version of the tubes task, marmosets preferred to look at events in which an object dropped down the tube was revealed in the gravity box. This suggests that they perceptually detected violations of continuity/solidity and did not expect the object to land in the unconnected box. However, marmosets apparently failed to apply their perceptual sensitivity to continuity/solidity constraints when searching for the object, since they were unable to spontaneously locate the object in Experiments 1 and 2. But even though they initially failed to find the object, they did not have a marked preference for the gravity box. Instead, some of them learned to localize the object, and in some instances, they were even able to transfer the solution when presented with a new tube configuration. Thus, rather unexpected the bias was found to be somewhat less robust in common marmosets as compared to cotton top tamarins who searched the gravity location persistently even after repeated trials (Hood et al., 1999). Overall, marmosets appeared remarkably flexible in this task. They learned associative strategies other than position learning (i.e., select the box with the tube attached) which was the predominant strategy in dogs and great apes, which might be partly due to subtle differences in the methods used (i.e., great apes were not confronted with multiple configuration switches). Moreover, we observed substantial inter-individual differences. Unsuccessful individuals did not perseverate instead they developed a preference for the middle box. Apparently, the inter-individual differences were at least partially due to sex differences with males outperforming females. However, the sample size was too small to allow any conclusive statements; future studies may address these questions. In sum, marmosets’ performance in the action task resembled that of great apes and dogs. Also in marmosets, the successful inhibition of gravity impulses yielded in substantial behavioral flexibility (i.e., the adoption of a greater range of search strategies) but not necessarily in correct performance. It is possible that marmosets showed

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higher inhibitory control in this task than the closely related but more impulsive cotton-top tamarins. In a direct experimental comparison, Stevens et al. (2005) showed that common marmosets outperform cotton-top tamarins’ inhibitory abilities as measured in delayed gratification and self-control tasks. The correlation of inhibitory control and bias frequency was only demonstrated for human children so far (Freeman et al., 2004; Hood et al., 2006), future studies may better explore this important question in nonhuman primates. Nevertheless, gravity responses were not absent in marmosets. At least initially they clearly preferred locations in the “gravity area” (i.e., gravity and middle box). This preference became more manifest after the removal of the middle box. This suggests that the impulse to reach below the release point occurred as a reaction to physical gravity, a reaction that may be suppressed with heightened inhibitory control. Thus taken together, the present results suggest a dissociation between marmosets’ performance in action and perception versions of the tubes task. Our results are in line with the findings of Santos and Hauser (2002) and Santos et al. (2006) who report similar dissociation in rhesus macaques and tamarins and add to the growing body of evidence suggesting the presence of action/perception dissociations in human and non-human primates (i.e., Cacchione and Krist, 2004; Hood et al., 2000a,b; Santos et al., 2006; Spelke et al., 1992). Two classes of explanations have been proposed to explain action/perception mismatches contending either conceptual continuity or discontinuity over development (Santos et al., 2006). Continuity explanations propose that children fail to act correctly not because they lack correct knowledge but because they are limited in their motor capacities (Diamond, 1991; Baillargeon et al., 1990; Hood and Willats, 1986; Keen, 2003; Munakata et al., 1997). In the case of marmosets, this explanation seems not sufficient. Even though inhibition failure may account for the observed biases in marmosets, it cannot account for the action/perception mismatch. Marmosets’ problems inhibiting gravity biases were not substantial, but nevertheless they did not spontaneously apply their continuity/solidity knowledge revealed in their looking pattern. This suggests that their expectations measured in the perception task may be based on knowledge that is generally not used in action. Further evidence that this may in fact be the case comes from studies which did not observe a release of solidity knowledge after the suppression of gravity biases (e.g., Cacchione and Call, 2010; Osthaus et al., 2003). Discontinuity theorists criticize the “rich” interpretation of perception-based measures as revealing full fledged explicit knowledge (Bogartz et al., 2000; Cashon and Cohen, 2000; Haith, 1998; Munakata, 2000; Munakata et al., 2000; Rivera et al., 1999; Schilling, 2000). They claim that poor performance in action tasks reflects infants’ limited or absent knowledge properties and that knowledge revealed by perception may not be sufficient to support action. However, knowledge which is never translated into action cannot be of adaptive value (Gómez, 2005). A solution to this apparent conflict is that knowledge revealed by perception is qualitatively different from knowledge revealed by action. For example, Munakata (2001) proposes that search requires “stronger” representations than looking time measures. Another possibility is that the tasks do not exert a similar amount of cognitive load to the participant (Keen et al., 2003). When looking at events, only post hoc judgments are required while successful search requires predicting the objects further trajectory after its disappearance from view. This might explain why “weak” representations suffice to support successful perception but fail to do so in case of action. Thus, it is possible that marmosets have some knowledge of object continuity/solidity, which is not strong enough to be translated into action. Therefore, the successful inhibition of gravity impulses results in

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greater behavioral flexibility but not in the adoption of solidity knowledge. In sum, common marmosets were not spontaneously successful in the tubes task. Nevertheless, presumably due to their advanced inhibitory abilities they behaved quite flexibly by adopting various search strategies. Marmosets’ behavior in the action task was in dissociation with their performance in a looking time version of the task, which suggests some sensitivity to object continuity/solidity. A shortcoming of the present studies is that they were not designed to disentangle what exactly the marmosets learned (i.e., developed a strategy to search for the box with the tube attached, or eventually gathered a rudimentary knowledge of the tubes’ causal function). Future research is needed to pinpoint how continuity/solidity constraints on the one hand and in naïve reasoning about gravity on the other hand govern looking and action across development. Acknowledgments We thank Marion Strasser and Urs Bachofner for data collection and analysis, and Heinz Galli for caring for the marmosets colony and assistance during the experiments. References Ahmed, A., Ruffman, T., 1998. Why do infants make A not B errors in a search task, yet show memory for the location of hidden objects in a non-search task? Dev. Psychol. 34, 441–445. Amici, F., Aureli, F., Call, J., 2008. Fission–fusion dynamics, behavioral flexibility and inhibitory control in primates. Curr. Biol. 18, 1415–1419. Baillargeon, R., 2002. The acquisition of physical knowledge in infancy: A summary in eight lessons. In: Goswami, U. (Ed.), Handbook of Childhood Cognitive Development. Blackwell, Oxford, pp. 47–83. Baillargeon, R., 2004. Infants’ reasoning about hidden objects: evidence for eventgeneral and event-specific expectations. Dev. Sci. 7, 391–424. Baillargeon, R., Graber, M., DeVos, J., Black, J., 1990. Why do young infants fail to search for hidden objects? Cognition 36, 255–284. Baillargeon, R., Kotovsky, L., Needham, A., 1995. The acquisition of physical knowledge in infancy. In: Sperber, D., Premack, D., Premack, A.J. (Eds.), Causal Cognition: a Multidisciplinary Debate. Clarendon Press, Oxford, pp. 79–116. Berthier, N., Deblois, S., Poirier, C.R., Novak, M.A., Clifton, R.K., 2000. Where’s a ball? Two and three year olds about unseen events. Dev. Psychol. 36, 394–401. Bogartz, R.S., Shinksey, J.L., Schilling, T.H., 2000. Object permanence in five-and-ahalf-month-old infants? Infancy 1, 403–428. Burkart, J.M., Heschl, A., 2007. Perspective taking or behaviour reading? Understanding of visual access in common marmosets (Callithrix jacchus). Anim. Behav. 73, 457–469. Cacchione, T., Call, J., 2010. Intuitions about gravity and solidity in great apes: the tubes task. Dev. Sci. 13, 320–330. Cacchione, T., Call, J., Zingg, R., 2009. Gravity and solidity in four great ape species (Gorilla gorilla, Pongo pygmaeus, Pan troglodytes, Pan paniscus): vertical and horizontal variations of the table task. J. Comp. Psychol. 123, 168–180. Cacchione, T., Krist, H., 2004. Recognizing impossible object relations: intuitions about support in chimpanzees (Pan troglodytes). J. Comp. Psychol. 118, 140–148. Cashon, C.H., Cohen, L.B., 2000. Eight-month-old infants’ perception of possible and impossible events. Infancy 1, 429–446. Deaner, R.O., van Schaik, C.P., Johnson, V., 2006. Do some taxa have better domaingeneral cognition than others? A meta-analysis of non-human primate studies. Evol. Psychol. 4, 149–169. Diamond, A., 1991. Neuropsychological insights into the meaning of object concept development. In: Carey, S., Gelman, R. (Eds.), The Epigenesis of Mind: Essays on Biology and Cognition. Erlbaum, New Jersey, pp. 67–110.

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