Do animals understand invisible displacement? A critical review.

Journal of Comparative Psychology 2014, Vol. 128, No. 3, 225–239

© 2014 American Psychological Association 0735-7036/14/$12.00 DOI: 10.1037/a0035675

Do Animals Understand Invisible Displacement? A Critical Review Kelly Jaakkola

This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.

Dolphin Research Center, Grassy Key, Florida The ability to mentally represent the movement of hidden objects (i.e., invisible displacement) is of theoretical importance due to its generally accepted status as an indicator of the development of a powerful type of representational capacity in human children. Over the past few decades, the understanding of invisible displacement has been claimed for a variety of animal species as well. However, a careful review of these studies finds that: (a) many were not properly blinded, (b) many did not properly control for lower-level associative strategies, and (c) success on simplified versions of the tasks can be explained by a simple attentional mechanism rather than by conceptual understanding. Indeed, when lower-level factors are controlled, evidence of understanding invisible displacement remains only for great apes. Keywords: invisible displacement, object permanence, secondary representation, comparative cognition

experiments have tracked infants’ abilities to first search for objects they’ve seen partially hidden, then objects they’ve seen fully hidden (called visible displacement), then finally, at around 18 to 24 months of age, to search for objects that are fully hidden and then moved to a second location (called invisible displacement; e.g., Harris, 1987; Marcovitch & Zelazo, 1999; Piaget, 1954).1 By definition, understanding invisible displacement requires the mental reconstruction of an event that has not been seen. That is, to know that an object arrived at a second location without actually seeing the object move there, the subject must mentally track or reconstruct the object’s possible movements. This is where the theoretical significance comes into play. In theories of cognitive development, the ability to understand invisible displacement is often viewed as an indicator of a new type of representational capacity in the developing child. Piaget (1954) described it as the beginning of symbolic thought. Perner (1991) described it as the beginning of secondary representation, or the ability to consider multiple models of a situation rather than a single model based on what is immediately perceivable. In both theories, passing the invisible displacement task is one of a cluster of abilities—including means-ends understanding, pretense, understanding of external representations, and mirror self-recognition—which are manifestations of this new type of representational capacity. More recently, the discussion about the representational implications of invisible displacement has been extended phylogenetically across the animal kingdom. Suddendorf and Whiten (2001) made the case that among nonhuman animals, great apes (and likely only great apes) possess the capacity for secondary representation, based partly on the fact that apes have shown clear evidence of passing invisible displacement tasks. It is important to note that this type of claim is not merely descriptive in nature, but carries profound implications for our understanding of the evolution of cognition. That is, our hypotheses about the possible

The ability to reason about the location and movements of hidden objects is a fundamental cognitive skill of both practical and theoretical significance. Because we live in a world where biologically relevant entities (such as predators, prey, and social partners) move, the ability to hold such objects in mind when they temporarily disappear from sight imparts obvious adaptive advantages. When a pursued mouse runs into a hole, or a mate moves behind a tree, for example, any animal that conceptualizes them as ceasing to exist would be at a profound disadvantage to an animal that conceptualizes them as existing out of sight, waiting to be found. However, all disappearances are not created equal. In some cases, the disappearing entity might (a) provide other perceptual clues to its location, such as odor or sounds. In other cases, it might (b) remain at the spot where it disappeared from view (e.g., an animal escaping into a knothole in a tree). In yet other cases, it might continue to move after disappearing from sight, either (c) continuing on its current trajectory (e.g., a predator passing behind a tree), or perhaps (d) moving with its occluder/container in a hidden state (e.g., a baby marsupial in its mother’s pouch). Importantly, the cognitive representations needed to reason effectively about the disappearing entity in each of these four cases are likely markedly different, involving an understanding of, respectively, (a) perceptually locating something, (b) visible displacement, (c) trajectory extrapolation, and (d) traditional invisible displacement. In humans, the development of the ability to reason about hidden objects has been extensively investigated. Hundreds of

This article was published Online First March 10, 2014. Kelly Jaakkola, Research department, Dolphin Research Center, Grassy Key, Florida. Many thanks to James Ha, Emily Guarino, Sara Chi, and three anonymous reviewers for helpful comments on earlier drafts of this article. Correspondence concerning this article should be addressed to Kelly Jaakkola, Dolphin Research Center, 58901 Overseas Highway, Grassy Key, FL 33050. E-mail: [email protected]

1 Note that the current review focuses specifically on studies in which understanding of hidden objects is assessed using measures of active search. I will address the issue of research that uses alternative looking time measures in the final discussion.

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selection pressures that give rise to a particular cognitive trait will necessarily be quite different depending on whether that trait is: (a) widespread across the animal kingdom; (b) shared among only closely related species (such as humans and apes); or (c) shared among a select group of unrelated species (such as apes, dolphins, and certain birds). Of course, to properly evaluate claims about the theoretical implications of success on a task across the animal kingdom, one must first have an accurate accounting of the performance of a wide variety of animal species. Over the past several decades, the phylogenetic map for this ability has begun to take shape. But while it is encouraging that testing on this task has moved beyond apes, and even beyond primates, it is unfortunate that many of these studies have failed to eliminate alternative explanations for success. In the 15 years or so since previous reviews of this area (e.g., Doré & Goulet, 1998; Tomasello & Call, 1997), advances have been made in experimental methodology, and new data have been reported for a number of species. The purpose of the current review is to critically evaluate each point on the phylogenetic map of invisible displacement ability across the animal kingdom, which will then allow us to evaluate the relevant theoretical claims.

Types of Tasks The understanding of invisible displacement in nonhuman animals has been assessed by three main experimental methodologies:

Standard Piagetian Task In this task, subjects are presented with an array of opaque containers (see Figure 1). The experimenter hides a target object inside a displacement device (such as a hand or small box), places the displacement device inside one of the opaque containers, and surreptitiously transfers the object to that container. The experimenter then removes the displacement device from the container and shows the subject that the device is empty, before allowing the subject to search for the object.2

Transposition In this task, the subject is again presented with an array of opaque containers (see Figure 2). The experimenter places the target object directly into one of these containers without an intermediating displacement device, then moves one or more of the containers. Depending on whether the containers cross paths and whether a previously empty container moves into the original location of the baited container, this transposition may take one of several forms: (a) simple lateral, in which the container(s) move

Figure 1. Schematic illustration of the standard Piagetian invisible displacement task. The dotted arrow represents the initial baiting of the object (circle) into the displacement device. The solid arrow represents the movement of the displacement device into the hiding container.

laterally and the original location of the baited container remains empty; (b) lateral substitution, in which the containers move laterally in such a way that an empty container moves into the original location of the baited container; (c) simple cross, in which the containers cross paths and the original location of the baited container remains empty; or (d) switch, in which the containers cross paths in such a way that an empty container moves into the original location of the baited container. As we shall see, some forms of transposition are much easier than others, and may reflect different underlying representations.

Rotation In this task, the experimenter places the target object directly into one of the opaque containers, then rotates the entire array on a turntable (see Figure 3). In the original version of this task, the turntable is rotated 180 degrees so that the array superficially appears the same both before and after the rotation. In a more recently introduced, simpler version, the array may only be rotated 90 degrees. Unfortunately, this 90-degree procedure has so far been implemented almost exclusively by placing one container directly in front of the animal, with the other behind it on the opposite side of the apparatus, partially occluded by the front container (Hoffmann, Rüttler, & Nieder, 2011; Miller, Gipson, Vaughan, Rayburn-Reeves, & Zentall, 2009; Miller, RayburnReeves, & Zentall, 2009). Because the experimenter always baits this front container, it may be that the animal simply tracks this single container in front of it, with no need to pay attention to the second container at all. The common factor in all three tasks (Piagetian, transposition, and rotation) is that the final movement of the target object is not perceptible to the experimental subject, but must be arrived at by logical inference over the animal’s mental representation of the situation. Beyond that commonality, each task carries distinct perceptual, memorial, and informational processing challenges which may differentially affect the results of the tests. For example, the Piagetian task involves both invisible movement and invisible transfer of the target object between containers. In contrast, transpositions and rotations eliminate the invisible transfer between containers (which might be thought to make the task easier) but involve more moving elements to keep track of (which might conceivably make the task more difficult). It is therefore not intuitively obvious which task might provide the purest assessment of understanding invisible displacement, with the least disruptive additional complicating factors. Empirically, it turns out that human children find the standard Piagetian task considerably easier than switch transpositions (Barth & Call, 2006; Sophian & Sage, 1983), whereas great apes find the two tasks comparable (Barth & Call, 2006). Both apes and children find the 180-degree rotation task the most difficult of all (Barth & Call, 2006). 2 Note that this specifically describes Piaget’s single invisible displacement task. Because this review is specifically concerned with the most basic understanding of invisible displacement, I have not included the more complicated successive invisible displacement tasks, which both presuppose and go beyond the mental resources required for this basic understanding.


DO ANIMALS UNDERSTAND INVISIBLE DISPLACEMENT?

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Figure 2. Schematic illustration of the four types of transformation task: (a) simple lateral, (b) lateral substitution, (c) simple cross, and (d) switch. The dotted arrow represents the initial baiting of the object (circle) into the hiding container. The solid arrows represent the subsequent movements of the containers.

Common Problems To claim that any species understands invisible displacement, it is crucial to first rule out possible confounding factors. In particular, there are at least three cue-based or associative strategies that, if not controlled, could account for an animal’s success on invisible displacement tasks without a conceptual understanding of invisible displacement.

Sensory Cues To ensure that the animal has tracked the invisible displacement, the target object must not be perceptible by any sensory modality at the time of searching. In animals known for their keen sense of

smell, such as dogs, this would seem to be an important consideration. Studies have addressed this possibility in a variety of ways, including: (a) palming the object rather than hiding it in the target location (e.g., Triana & Pasnak, 1981); (b) rubbing the target object or enclosing duplicate objects in each of the hiding places before testing (e.g., Collier-Baker, Davis, & Suddendorf, 2004; Gagnon & Doré, 1992; Miller, Gipson, et al., 2009); and (c) spraying a masking odor or scattering food bits over the entire apparatus (e.g., Deppe, Wright, & Szelistowski, 2009; Doré, Fiset, Goulet, Dumas, & Gagnon, 1996; Fiset & LeBlanc, 2007; Funk, 1996; Gagnon & Doré, 1992). It is perhaps worth noting, however, that studies which have explicitly tested whether dogs utilize olfactory cues to succeed in invisible displacement and other

Figure 3. Schematic illustration of the (a) 180-degree and (b) 90-degree rotation tasks. The dotted arrow represents the initial baiting of the object (circle) into the hiding container. The solid arrows represent the subsequent rotation of the platform.


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similar types of hidden-object tasks have found that they do not (e.g., Bräuer, Kaminski, Riedel, Call, & Tomasello, 2006; Gagnon & Doré, 1992; Miklósi, Polgárdi, Topál, & Csányi, 1998). Therefore, although problematic in theory, it seems unlikely that olfactory cues have played a large role in creating false positive claims. Certainly in studies of animals not known for their keen sense of smell (such as primates, dolphins, and birds), odor controls are rarely employed and likely unnecessary. Similarly, in animals possessing the ability to echolocate (e.g., dolphins, bats), it is essential to ensure that the hidden object is not perceivable via echolocation. In dolphins, this has been controlled by conducting the experiment in air rather than underwater (Jaakkola, Guarino, Rodriguez, Erb, & Trone, 2010). Alternatively, one could utilize containers that are not penetrable by echolocation (i.e., that are acoustically opaque). Finally, some experiments use magnetic dishes and magnets to hold and displace the hidden objects (e.g., Auersperg, Szabo, von Bayern, & Bugnyar, 2013; de Blois, Novak, & Bond, 1998; Doré, 1986, 1990). For most animals, this may not be an issue, but for animals with the ability to detect magnetic fields, such as may be common across many bird species (e.g., Goodenough, McGuire, & Jakob, 2010; Wiltschko & Wiltschko, 2006), this is an important consideration.

Social Cues Since the phenomenon of Clever Hans, a horse once thought to be able to read, count, and solve mathematical equations (Pfungst, 1911), comparative psychologists have been acutely aware of the dangers of accidental social cueing. Typically, this is addressed by using blinding protocols to ensure that the animal cannot see the experimenter at the time of testing, and/or that the experimenter is unaware of what the correct response should be. The point is to make it impossible for the animal to deduce the answer by reading unintentional body language. However, in face-to-face procedures such as those employed in invisible displacement tasks, such blinding can be difficult. Researchers have attempted to control for social cueing in a number of ways, including: (a) fixing the experimenter’s gaze away from the testing display (e.g., at the floor or wall) after she performs the invisible displacement manipulation (e.g., Deppe et al., 2009; Doré et al., 1996; Fedor, Skollár, Szerencsy, & Ujhelyi, 2008; Neiworth, Steinmark, Basile, Wonders, Steely, & DeHart, 2003); (b) shielding the experimenter’s eyes with sunglasses, a baseball cap, or a welder’s mask (e.g., Call, 2001, 2003; Collier-Baker, Davis, Nielsen, & Suddendorf, 2006; de Blois & Novak, 1994); (c) concealing part or all of the experimenter’s body behind a screen (e.g., Collier-Baker et al., 2004; Fiset & LeBlanc, 2007; Funk, 1996); or (d) utilizing one experimenter to perform the invisible displacement manipulation, and a second, blind experimenter to present the experimental array to the animal (e.g., Beran & Minahan, 2000; Jaakkola et al., 2010). Other researchers have taken the position that blinding is not a major concern for several reasons. First, they suggest that because a face-to-face procedure is standard for these types of tasks, any social cueing will occur equally for all species tested, and therefore any differences between species will be due to something other than this common factor of cueing (e.g., Gagnon & Doré, 1992; Pepperberg & Kozak, 1986; Pepperberg & Funk, 1990). This argument is problematic for two reasons. First, as just reviewed,

some experiments do build blinding protocols into their procedures. Second, and more troublesome, is the inherent assumption that all species are equally adept at picking up potential human cues, which is simply not the case (e.g., Bräuer et al., 2006; Miklósi & Soproni, 2006). Therefore, even among animals tested with the same nonblind procedure, differences between species could be due either to differences in understanding invisible displacement, or to differences in understanding human cues. Some authors, citing Triana and Pasnak’s (1981) study with dogs and cats, have claimed that even obvious social cueing such as pointing does not help subjects who lack the cognitive abilities to pass invisible displacement tasks (e.g., Gagnon & Doré, 1992; Pepperberg, 2002; Pepperberg, Willner, & Gravitz, 1997; Pepperberg & Funk, 1990; Pepperberg & Kozak, 1986). Therefore, the unstated assumption goes, more subtle social cues should not help either. However, recent studies have shown that cats and especially dogs are able to use human pointing as a cue to locate hidden objects (see Miklósi & Soproni, 2006 for a review). Moreover, the assumption that pointing should be the most salient social cue for the animal subjects, as it is for humans, is also unfounded. A particular animal species might fail to understand pointing, yet intuitively understand gaze, breath holding, body tension, or other possible experimenter cues. To mitigate the problem of accidental social cueing, some studies have utilized several experimenters in order to give the subject animals less opportunity to learn the idiosyncratic cues of any particular experimenter (e.g., Pepperberg & Kozak, 1986; Pepperberg et al., 1997). Although this strategy acknowledges one possible form of cueing, it fails to address the more difficult issue of general attentional indicators or body language that experimenters naturally share. After all, the beauty of the original Clever Hans phenomenon was that the horse’s performance did not depend on any one specific trainer (Pfungst, 1911). Finally, some researchers have argued that if an animal passes a successive invisible displacement task such as Uzgiris and Hunt’s (1975) Task 15, this provides prima facie evidence that no cueing was involved (e.g., Pepperberg, 2002; Pepperberg & Kozak, 1986; Pepperberg et al., 1997). In this task, the experimenter first hides the target object in her hand, drops the object at the first hiding place, but then continues to move her hand into the other hiding places as well, purportedly leading the animal to believe that the object is hidden in the final location. The argument goes that if the subject searches in the final location (where the object should be), rather than in the first location (where the experimenter knows it to be), there must have been no cueing. This reasoning is also problematic. It is not unreasonable to assume that the experimenter might unconsciously cue the correct answer (i.e., where he or she expects the animal should search) rather than the location where the object actually is. Despite the above reservations, it is important to acknowledge the possibility that animals in these uncontrolled studies may not solve invisible displacement problems by reading social cues. However, the point is that this cannot be our default assumption. When animals pass these tests, we attribute to them an understanding of invisible displacement, which might just be a more remarkable claim than the idea that they can interpret body language. It is therefore incumbent on us to show not only that the animals are probably not solving the tasks any other way, but that they could not possibly solve them any other way.



Associative Learning Even in the absence of sensory and social cues, an animal might pass invisible displacement tasks by learning simple associational rules such as pick the location that the experimenter indicated (e.g., Doré & Dumas, 1987; Natale, Antinucci, Spinozzi, & Potì, 1986). This consideration is especially critical in extended testing protocols such as Uzgiris and Hunt’s commonly used (1975) procedure, which systematically tests easier, visible displacement problems before gradually working up through the more difficult invisible displacement problems (e.g., Gagnon & Doré, 1992). One strategy to mitigate this problem involves limiting the number of trials presented to the animal (Doré & Dumas, 1987). After all, if an animal consistently solves the task after just three or four trials, it is much less likely to have learned an associative rule than if it consistently solves the task only after 20 or 30 trials. Often overlooked, however, is the notion that this trial limit must include all trials that are solvable by a given rule, regardless of whether those trials are part of the same experimental condition. For example, suppose an animal receives four trials in each of the following experimental conditions: (a) visible displacement with a single hiding place; (b) visible displacement to the same location repeatedly among several hiding places; (c) visible displacement to varying locations among several hiding places; (d) invisible displacement with a single hiding place; and (e) invisible displacement with several hiding places. Even if the animal solves the invisible displacement choice (Condition E) on the “first trial,” it would have first experienced 16 trials on which it could have learned an associative rule. A second strategy some experimenters have used to mitigate the possibility of associative learning has been to touch one or more of the nonbaited containers after the object is hidden, ensuring that the animal cannot succeed by using the rule, pick the last location touched (e.g., Funk, 1996; Zucca, Milos, & Vallortigara, 2007). To be sure, this is a step in the right direction. However, this strategy speaks only to one very specific associative learning rule. It does nothing to address other possible associational rules, such as pick the last location where the cover was lifted (or whatever movement was used during hiding) or pick the first location touched. Finally, a third strategy has been to run systematic controls in which identical hiding motions are performed at more than one location. For example, in what might be termed the drop-first control, the experimenter hides the object inside a displacement device, places the device in one of the containers, and transfers the object to that container. Then the experimenter removes the displacement device from the container, shows the subject that the device is empty before placing it into a second container. The crucial feature of this procedure is that the experimenter interacts identically with the baited and distractor containers, thus controlling for the possibility that the animal is simply choosing the last container that was indicated in any way (e.g., Collier-Baker et al., 2004, 2006; de Blois & Novak, 1994; de Blois et al., 1998; Jaakkola et al., 2010; Mendes & Huber, 2004; Neiworth et al., 2003; Pepperberg et al., 1997). However, even controlling for the last indicated rule is not sufficient to rule out associative learning. During the standard invisible displacement task, the experimenter interacts with only a single container. There is no need for an animal to disambiguate this container as the first or last indicated until it is confronted with

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a situation in which more than one container is indicated, at which point it may choose to disambiguate one way or the other. Therefore, one also needs a second control procedure in which the distractor container is indicated before the target object is hidden. In this drop-last procedure, the experimenter hides the object in a displacement device, places this device inside one of the containers, then takes it out again and shows the subject that the object is still in the device. He then hides the object within the device again, places the device in a second container, and transfers the object to the second container before removing the displacement device and showing the subject that the device is now empty. This procedure thus controls for the possibility that the animal is choosing the first container indicated in any way (e.g., Auersperg et al., 2013; Collier-Baker et al., 2004, 2006; Jaakkola et al., 2010; Neiworth et al., 2003). Unfortunately, this drop-last control has been employed much less frequently than its drop-first counterpart, leaving the issue of associative learning only partially controlled in most studies. It is important to note that although the drop-last control is similar in structure to the more common successive invisible displacement task, these two tasks are not interchangeable. In both cases, the displacement device moves successively into two or more locations. However, in successive invisible displacement, the object remains invisibly hidden inside the displacement device between hiding places, leading to a situation in which the final hiding place of the target object is ambiguous. Because of this ambiguity, subjects are permitted to search at multiple locations so long as each location searched is one of the hiding places visited by the device. Therefore, unlike the case with the drop-last control, an animal who is following an associative strategy of simply searching at the location(s) the device visited could theoretically pass this task, making it an ineffective control for such strategies.

Empirical Studies Invisible displacement has been tested in a variety of animal species, including birds, cats, dogs, dolphins, lemurs, monkeys, and apes (summarized in Tables 1, 2, and 3). In the following sections, I systematically review the evidence for understanding in each of these animal groups.

Birds Piagetian task. To date, nine species of birds—four from the psittacid family (African Grey parrots, Illiger mini macaws, cockatiels, and New Zealand parakeets) and five from the corvid family (magpies, Eurasian jays, carrion crows, common ravens, and jackdaws)— have been tested on the Uzgiris-Hunt scale of object permanence (Bugnyar, Stöwe, & Heinrich, 2007; Funk, 1996; Hoffmann et al., 2011; Pepperberg & Funk, 1990; Pepperberg & Kozak, 1986; Pepperberg et al., 1997; Pollok, Prior, & Güntürkün, 2000; Ujfalussy, Miklósi, & Bugnyar, 2013; Zucca et al., 2007). In this procedure, which was first developed for human infants, subjects are presented with an array of increasingly difficult object displacement tasks, including: visual pursuit of a moving object; single visible displacement with an increasing number of hiding places; multiple visible displacement; visible displacement under multiple overlapping screens; single invisible displacements with an increasing number of hiding places; and multiple invisible displacements. All eight species have succeeded on all tasks,

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Table 1 Summary of Animal Invisible Displacement Studies Using the Standard Piagetian Task Study

Pass task?

Blinding?

Pepperberg & Kozak (1986) Pepperberg & Funk (1990) Funk (1996) Pepperberg et al. (1997) Pollok et al. (2000) Zucca et al. (2007) Bugnyar et al. (2007) Hoffman et al. (2011) Ujfalussy et al. (2013) Auersperg et al. (2013)

Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes

Birds No No Yes No No Uncleara Yes Yes No Yes

Triana & Pasnak (1981) Doré (1986) Dumas & Doré (1989) Doré (1990) Goulet et al. (1994)

Yes No No No No

No No No No No

Triana & Pasnak (1981) Gagnon & Doré (1992) Gagnon & Doré (1993) Collier-Baker et al. (2004) Fiset & LeBlanc (2007)

Yes Yes Yes No No

No No No Yes Yes

Jaakkola et al. (2010)

No

Yes

Deppe et al. (2009) Mallavarapu et al. (2013)

No No

Yes Yes

Wise et al. (1974) Mathieu et al. (1976) Natale et al. (1986) Schino et al. (1990) de Blois & Novak (1994) de Blois et al. (1998) Neiworth et al. (2003) Mendes & Huber (2004)

Yes Yes No Yes No No Yes Yes

No No No No Yes No Yes No

Fedor et al. (2008)

Yes

Yes

Mathieu et al. (1976) Redshaw (1978) Wood et al. (1980) Natale et al. (1986) de Blois et al. (1998) Call (2001) Barth & Call (2006) Collier-Baker et al. (2006)

Yes Yes Yes Yes Yes Yes Yes Yes

No No No No No Yes Nod Yes

Associative controls?

Demonstrates understanding?

No No Incomplete Incomplete No Incomplete No No No Yes

Indeterminate Indeterminate Indeterminate Indeterminate Indeterminate Indeterminate Indeterminate Indeterminate Indeterminate Indeterminateb

No No No No No

Indeterminate No No No No

No No No Yes No

Indeterminate Indeterminate Indeterminate No No

Yes

No

No Incomplete

No No

No Yesc Incomplete Incomplete Incomplete No Failed No

Indeterminate Indeterminate No Indeterminate No No No Indeterminate

Incomplete

Indeterminate

Yesc No No Incomplete Incomplete No No Yes

Indeterminate Indeterminate Indeterminate Indeterminate Indeterminate Indeterminate Indeterminate Yes

Cats

Dogs

Dolphins Prosimians

Monkeys

Lesser apes Great apes

Note. Blinding was coded as Yes if any reasonable attempt at blinding was made (e.g., The experimenter looked away, wore sunglasses, hid, was blind to the correct answer). Associative controls was coded as Yes if both drop-first and drop-last controls were passed, Failed if the animals failed one or more of these controls, Incomplete if less than the full set of controls was administered, and No if no control was administered. Demonstrates Understanding was coded as Yes if any animal passed the task and the study included all the necessary controls, Indeterminate if the animals passed the task but the study did not include all the necessary controls, and No if the animals failed the task. For space purposes, specific species of birds, monkeys, and apes are collapsed in the table. a See Footnote 3. b The hidden object may have been perceivable via magnetoreception. c Excessive number of trials still opens possibility of associative learning. d Differential success across tasks argues against inadvertent social cues.


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Table 2 Summary of Animal Invisible Displacement Studies Using the Transposition Task Study

Transposition type

Blinding?


Yes Yes No Yes Yes

No Uncleara Yes No Yes

Indeterminate Indeterminate No Indeterminate Indeterminateb

Pass task? Birds

Pepperberg et al. (1997) Zucca et al. (2007) Hoffman et al. (2011) Ujfalussy et al. (2013) Auersperg et al. (2013)

Switch Switch Switch Simple cross Switch

Doré et al. (1996)

Simple lateral, lateral substitution, switch

Pass simple lateral; fail others

Yes

No

Doré et al. (1996) Rooijakkers et al. (2009) Fiset & Plourde (2013)

Dogs Simple lateral, lateral substitution, switch Simple lateral, simple cross, lateral substitution, switch Simple lateral, lateral substitution

Pass simple lateral; fail others Pass simple lateral; fail others Pass simple lateral; fail others

Yes No No

No No No

Jaakkola et al. (2010)

Simple cross

No

Yes

No

Anderson (2012)

Switch

Yes

No

Indeterminate

Beran & Minahan (2000) Call (2003) Barth & Call (2006) Rooijakkers et al. (2009)

Great apes Switch Switch Switch Simple lateral, simple cross, lateral substitution, switch

Yes Yes Yes Yes

Yes Yes Noc No

Yes Yes Yes Indeterminate


Cats

Dolphins Prosimians

Note. Blinding was coded as Yes if any reasonable attempt at blinding was made (e.g., The experimenter looked away, wore sunglasses, hid, was blind to the correct answer). Demonstrates Understanding was coded as Yes if any animal passed the task and the study included all the necessary controls, Indeterminate if the animals passed the task but the study did not include all the necessary controls, and No if the animals failed the task. For space purposes, specific species of birds and apes are collapsed in the table. a See Footnote 3. b The hidden object may have been perceivable via magnetoreception. c Differential success across tasks argues against inadvertent social cues.

suggesting that they understand invisible displacement. However, inadequate controls in all of these studies make such a claim suspect. Although several studies implemented procedures to guard against unintentional social cueing (Bugnyar et al., 2007; Funk, 1996; Hoffmann et al., 2011), none controlled adequately for associative learning. In two of the studies (Funk, 1996; Zucca et al., 2007), the experimenter touched multiple covers after the object was hidden. However, as mentioned previously, touch alone is inadequate to rule out associative learning. Only one study (Pepperberg et al., 1997) included the drop-first control, but because they did not also administer the complementary drop-last control, the possibility remains that the birds may have been using the alternate rule of picking the first touched hiding place. An additional study (Auersperg et al., 2013) tested Goffin cockatoos on both visible and invisible displacement tasks. Surprisingly, seven of the eight birds showed considerable difficulty passing the first visible displacement task in which the object was fully hidden (i.e., Stage 5A). Once they solved this, however, all of the birds immediately passed more complicated visible displacement problems, and two of them eventually moved on to pass invisible displacement problems including both drop-first and drop-last controls. Unfortunately, however, the hidden object was always located on a dish with a magnet attached (so the experimenters could displace the object using another magnet beneath the table). Because the ability to perceive magnetism is a sense common across a variety of birds (e.g., Goodenough et al., 2010;

Wiltschko & Wiltschko, 2006), this opens the possibility that these birds may have been directly perceiving the location of the magnet, rather than understanding invisible displacement. Transpositions. Five studies have administered switch transposition tasks to birds. In one (Hoffmann et al., 2011), crows failed this task. The other studies reported that African Grey parrots (Pepperberg et al., 1997), Eurasian jays (Zucca et al., 2007), jackdaws (Ujfalussy et al., 2013), and Goffin cockatoos (Auersperg et al., 2013) passed. Unfortunately, the experimenters in the first three of these tests were not blinded,3 and the fourth test may have been solvable by birds’ magnetoreception. Rotations. Finally, two studies have also utilized a rotation task. In the first (Hoffmann et al., 2011), crows were presented with two opaque containers on either side of a round wooden platform. One container was baited, and the platform was rotated 90, 180, or 360 degrees. The crows succeeded at 90 degrees, but 3 Zucca et al.’s (2007) procedure states that the experimenter “never looked at the experimental setup during the administration of the task,” leaving it unclear how he or she was able to perform the task manipulations. A clearer description is needed to rule out inadvertent cueing. In addition, this study suffers from a severe underreporting of procedure, making the results difficult to interpret. For example, the supplementary video of this task shows the target object being hidden behind a screen of a different color than the incorrect screens, opening the possibility that the birds were tracking the differently colored screen rather than the movement of the object hidden behind it.

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Table 3 Summary of Animal Invisible Displacement Studies Using the Rotation Task Study

Rotation type

Pass task?

Blinding?


Pass 90; fail others Yes

Yes Yes

No Indeterminatea

Pass 90; fail 180 Pass 90

No No

No Indeterminate

Yes Yes Yes With landmarks Yes

Yes Yes Nob Yes No

Yes Yes Yes Indeterminatec Indeterminate

Birds Hoffman et al. (2011) Auersperg et al. (2013)

90, 180, 360 90, 180, 270, 360

Miller, Gipson et al. (2009) Miller, Rayburn-Reeves et al. (2009)

90, 180 90

Beran & Minahan (2000) Call (2003) Barth & Call (2006) Okamoto-Barth & Call (2008) Albiach-Serrano (2010)

180 180 180 180, 360 180

Dogs


Great apes

Note. Blinding was coded as Yes if any reasonable attempt at blinding was made (e.g., The experimenter looked away, wore sunglasses, hid, was blind to the correct answer). Demonstrates Understanding was coded as Yes if any animal passed the task and the study included all the necessary controls, Indeterminate if the animals passed the task but the study did not include all the necessary controls, and No if the animals failed the task. For space purposes, specific species of birds and apes are collapsed in the table. a The hidden object may have been perceivable via magnetoreception. b Differential success across tasks argues against inadvertent social cues. c Due to the landmarks, this may not be a true test of invisible displacement.

failed at the larger rotations. Because the containers in the 90degree condition were arranged directly in line with the subject (see Figure 3b), this suggests that the crows may have simply tracked the container in front of them rather than systematically tracking the movement of the hidden object. In the second study (Auersperg et al., 2013), Goffin cockatoos were presented with three opaque containers on a platform which was rotated 90, 180, 270, or 360 degrees. As a group, the cockatoos passed all of these conditions. However, as with the standard Piagetian and transposition tasks in this same study, we cannot rule out the possibility that the birds could have been directly perceiving the magnet on which the hidden object was located.

Cats Piagetian task. Two early studies suggested that cats might understand invisible displacement. In the first, Triana and Pasnak (1981) presented cats with a truncated version of the Uzgiris-Hunt procedure, consisting of several visible and invisible displacement tasks in increasing order of difficulty. When the hidden object was food, cats succeeded at invisible displacement. This cannot be explained by odor cues because the experimenter surreptitiously palmed the food during hiding, leaving no actual food at the correct location. However, this study had no blinding procedure and no control for associative strategies. In the second study, Dumas (1992) used what he called a more ecological test of object permanence in which cats first saw the target object through a window, near the outside edge of one of two screens. To reach the object, the cat had to walk around an opaque barrier, during which time the object was moved behind the screen. Cats solved this task easily. However, contrary to Dumas’ claims, no understanding of invisible displacement was necessary. Because the object was always hidden behind the screen it had been nearest, the cats simply had to search at the last place they had seen the object (Goulet, Doré, & Rousseau, 1994).

In contrast to these early studies, later studies have suggested that cats do not understand invisible displacement. First, using a set of tasks similar to those of Triana and Pasnak (1981), Doré (1986, 1990; Dumas & Doré, 1989) found that cats succeeded at visible, but failed invisible, displacement tasks. Unfortunately, because Doré’s procedure modified the standard task such that the displacement container stopped in front of the hiding screen rather than moving behind it, this meant that the hiding screen was no longer a logically necessary place for the object to have moved, leaving it unclear that this was a true test of invisible displacement (Pasnak, Kurkjian, & Triana, 1988). However, when Goulet et al. (1994) eliminated this issue, cats were still unable to succeed at invisible displacement. Transpositions. When cats were tested on transpositions (Doré et al., 1996), they succeeded only in the case of simple lateral transpositions in which the original correct location remained empty. Cats failed if containers crossed paths, or if an empty container moved into the original location of the baited container, showing that they were unable to reliably track the movement of the hidden object.

Dogs Piagetian task. As with cats, early studies suggested that dogs might understand invisible displacement. Dogs succeeded on both a truncated version of the Uzgiris-Hunt procedure (Triana & Pasnak, 1981; Gagnon & Doré, 1992), and on tests of single visible and invisible displacements without this incremental procedure (Gagnon & Doré, 1992, 1993). Unfortunately, none of these studies included blinding procedures or controls for associative strategies. In contrast to these early apparent successes, later studies have suggested that dogs do not understand invisible displacement. Collier-Baker, Davis, and Suddendorf (2004) presented dogs with standard visible and invisible displacement problems using strict



controls, including hiding the top half of the experimenter behind a screen to control for experimenter cues, and utilizing both drop-first and drop-last procedures. They also systematically controlled the final placement of the displacement device. Under these stringent conditions, dogs’ performance on invisible displacement was no longer reliable. Rather, the best predictor of dogs’ search location was the final location of the displacement device. This could not simply be explained by an inability to inhibit searching at the location in which they saw the object disappear, because if the experimenters removed the displacement device entirely before the dogs searched, performance suffered. Without the cue of a displacement device, the dogs were simply at a loss for where to search. Fiset and LeBlanc (2007) also presented dogs with standard visible and invisible displacement problems, this time varying whether the experimenter was visible or concealed behind a barrier. They did not perform controls for associative learning, but did analyze their results systematically on the basis of the final location of the displacement device. Confirming Collier-Baker et al.’s (2004) results, dogs’ search patterns were primarily based on the location of the displacement device. Transpositions. Three studies have tested dogs’4 understanding of invisible displacement with transposition tasks (Doré et al., 1996; Fiset & Plourde, 2013; Rooijakkers, Kaminski, & Call, 2009). In all of them, dogs succeeded only in the simplest transpositions consisting of lateral movement in which the original correct location remained empty. Like cats, dogs failed if containers crossed paths or if an empty container was moved into the original location of the baited container, showing that they were unable to track the movement of the hidden object. Rotations. Finally, two studies utilized a rotation task in which dogs were presented with two buckets on either side of a wooden beam (Miller, Gipson, et al., 2009; Miller, RayburnReeves, et al., 2009). After one of the buckets was baited, the entire beam was rotated either 90 or 180 degrees. Like crows, the dogs succeeded at the 90 degree rotation, but failed at 180 degrees, suggesting that they may have simply tracked the container in front of them, rather than systematically tracking the movement of the hidden object.

Dolphins Piagetian task. In the only study so far to test dolphins (or any other marine mammals) on object permanence, Jaakkola et al. (2010) presented dolphins with visible and invisible displacement tasks, using strict controls, including a blinded experimenter and both drop-first and drop-last procedures. The dolphins passed visible displacement, and seemed to pass invisible displacement when a hand rather than a cylinder was used as the displacement device. However, the dolphins failed the drop-first and drop-last controls, showing that their apparent success was due to learned associative rules rather than a representational understanding of invisible displacement. Transpositions. Jaakkola et al. (2010) also tested the dolphins on a cross transposition task, which the dolphins failed, providing further evidence that they do not understand invisible displacement.

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Prosimians Piagetian task. To date, two studies have tested prosimians (specifically lemurs) on a series of visible and invisible displacement tasks (Deppe et al., 2009; Mallavarpu, Perdue, Stoinski, & Maple, 2013). The lemurs uniformly passed the visible, but failed the invisible displacement tasks (Deppe et al., 2009) or failed the control for associative strategies (Mallavarpu et al., 2013).

Monkeys Piagetian task. In the first study to test monkeys on invisible displacement, Wise, Wise, and Zimmerman (1974) presented two rhesus monkeys longitudinally with a series of increasingly difficult visible and invisible displacement tasks, which both monkeys eventually passed. However, there was no blinding and no control for learned associative rules. Two years later, Mathieu, Bouchard, Granger, and Herscovitch (1976) tested a capuchin and a woolly monkey on visible and invisible displacement. The woolly monkey passed only visible displacement, but the capuchin passed invisible displacement as well. Interestingly, in each trial, the displacement device visited each hiding place, leaving the object behind one of them, and revealed whether it still held the object after each location. Thus, drop-first and drop-last controls were included within the standard trials. Unfortunately, the excessive number of trials tested (60 per condition) opens the possibility that the capuchin could still have learned an associative rule such as pick the box visited after the target disappears. In addition, the experimenter was not blinded, leaving open the possibility of accidental cueing. When Natale, Antinucci, Spinozzi, and Potì (1986) tested a Japanese macaque on invisible displacement, it quickly learned to search under the correct container, but also searched under a container that was simply lifted even when the displacement device never moved close to that container, showing that it was following an associative rule. In a follow-up study, Schino, Spinozzi, and Berlinguer (1990) tested crab-eating macaques and capuchin monkeys on invisible displacement and this same lift control. One capuchin seemed to pass, primarily searching under the correct hiding spot in the invisible displacement task, but under the displacement device in the lift control, leading the authors to claim that he understood invisible displacement. Note, however, that an associative rule such as pick the hiding place that the displacement device interacts with, would explain these results. Also, the experimenter was not blinded, so the possibility of unintentional cueing cannot be ruled out. In contrast to these earlier claimed successes, two studies by de Blois and Novak (1994; de Blois et al., 1998) found that monkeys were unable to pass invisible displacement tasks. In the first (de Blois & Novak, 1994), rhesus monkeys did eventually learn to pass the task, but a closer look at their performance led the authors to conclude that this apparent success was the result of learned associative strategies. Squirrel monkeys failed a similar battery of tests (de Blois et al., 1998). Next, Neiworth et al. (2003) found that cotton-top tamarins passed an increasingly difficult series of visible and invisible 4 The Fiset and Plourde (2013) study tested wolves as well as dogs. The results for the two species were identical.


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displacement tasks. Although such a graded series is a prime candidate for teaching associative strategies, Neiworth et al. discount this possibility because the monkeys’ performance got worse, rather than better, as the tasks progressed. But this argument is unconvincing due to the fact that the tasks also got progressively more difficult. A decrease in performance should be expected, and learning could have been reflected as a boost in performance relative to difficulty. The monkeys also failed the drop-first control, which specifically tests for learned associative rules. Finally, Mendes and Huber (2004) reported that a small subset of marmosets passed a series of visible and invisible displacement tasks. However, the experimenter was not blinded. In addition, the authors attempted to address the issue of associative learning by reanalyzing their results using only the first six trials of each condition, but because associative learning can accumulate across conditions, this analysis doesn’t rule out the problem. The marmosets received 93 trials of visible displacement before they were tested on invisible displacement, then failed the crucial test that involved switching to a new hiding place—a test that should have been simple if they understood invisible displacement.5

Lesser Apes Piagetian task. To date, only a single study has used the Piagetian task to examine understanding of invisible displacement in lesser apes, also known as gibbons (Fedor et al., 2008). In this study, one of 10 subjects passed invisible displacement and the drop-first control. However, because the complementary drop-last control was not administered, we cannot rule out the possibility that the gibbon may have used the rule of picking the first touched hiding place. Transpositions. A second study tested gibbons’ understanding of switch transpositions, which the gibbons passed (Anderson, 2012). However, the experimenter was not blinded, and the excessive number of trials (132, including trials on which the gibbons were explicitly trained) raises the possibility of learned associative strategies.

Great Apes Piagetian task. In the first study to test these concepts with apes, Mathieu et al. (1976) tested a chimpanzee (along with a capuchin and woolly monkey, described earlier) on visible and invisible displacement, using built-in drop-first and drop-last procedures within the standard trials. Like the capuchin, the chimp passed all tests. However, the experimenter was not blinded, and the excessive number of trials leaves open the possibility of associative learning. The next two studies tested infant gorillas and chimpanzees longitudinally on the Uzgiris-Hunt scale of object permanence (Redshaw, 1978; Wood, Moriarty, Gardner, & Gardner, 1980). All subjects passed all tasks, but neither study controlled for unintentional social cues or associative learning. Natale et al. (1986) tested a gorilla on a series of invisible displacement tasks. When the color and size of the hiding containers changed across trials (to make it more difficult for the gorilla to identify simple patterns), the gorilla tended to search the displacement device and then the appropriate container. In control

trials in which the hiding container was simply lifted without the displacement device moving close to it, the gorilla searched the displacement device. The authors interpreted these results as evidence for a representational understanding of invisible displacement. However, the gorilla could have been following a simple rule of selecting the locations in the order in which the experimenter manipulated them (displacement device and then container). To rule this out, a drop-last control (in which the locations of early manipulations are incorrect) would be necessary. In the first object permanence test with orangutans (de Blois et al., 1998), the orangutans passed both visible and invisible displacement tasks, including a drop-first control. Unfortunately, without the complementary drop-last control, the possibility remains that the orangutans could have been following the associative rule of picking the first hiding spot manipulated. Call (2001) found that orangutans and chimpanzees passed single and double visible and invisible displacement tasks. However, this study failed to control for associative strategies. Five years later, Barth and Call (2006) tested all four great ape species on a standard invisible displacement task, which the apes passed at high levels. Although they included no controls for experimenter cueing, Barth and Call reasonably argue that because the apes showed differential success across this task, transpositions, and rotations (discussed in the next section), their performance could not be explained by inadvertent social cues. Unfortunately, this study also failed to control for associative rules, which are likely task-specific and therefore not subject to the same argument. Finally, Collier-Baker, Davis, Nielsen, and Suddendorf (2006) tested chimpanzees on standard invisible displacement with stringent controls, including outfitting the experimenter in a welder’s mask with white tape covering the transparent visor so the chimpanzees could not see her eyes, and utilizing both drop-first and drop-last procedures. The chimps performed extremely well, showing that they could solve the invisible displacement task without the use of lower-level associative strategies. Transpositions and rotations. In the first study to test apes (chimpanzees and bonobos) on transpositions and rotations, Beran and Minahan (2000) hid a piece of food under one of three cups, then either switched the position of the baited cup with another cup or rotated the entire array 180 degrees. To control for possible experimenter cues, the first experimenter turned away after the switch or rotation was made on some trials, and a second experimenter who had not seen the baiting pushed the tray forward. The apes passed all tests at high levels. However, these apes had been raised by humans in language-enriched rearing environments, and because this type of enculturation has been suggested to affect cognitive abilities (e.g., Furlong, Boose, & Boysen, 2008; Tomasello & Call, 2004; Van Schaik & Burkart, 2011), it is perhaps 5 Two of 11 subjects also seemed to pass a double invisible displacement test, but unfortunately, the authors did not report the results of the crucial control trials (in which a third location was also visited) separately from the standard trials, other than a statement that “roughly the same proportions of errors” occurred overall. However, because most monkeys failed this test, these “same proportions of errors” are not reassuring. What is crucially missing is an accurate reporting of the rates for the relevant two subjects, without which it is impossible to determine whether or not they used an associative strategy such as choose the last location visited.



worth considering whether these results generalize to nonenculturated apes. They do. Call (2003) also examined apes’ performance on switch transpositions and 180-degree rotations, this time with chimpanzees and orangutans. Like in Beran and Minahan’s (2000) study, all of the apes passed the tests at high levels. And because only two apes (out of six) had been raised with extensive human contact, this suggests that success on these tasks is also typical of nonenculturated apes. Three years later, Barth and Call (2006) tested all four great ape species on switch transpositions and 180-degree rotations, as well as on Piagetian invisible displacement (described earlier). The apes passed all tasks, but performed significantly worse on the rotations than on the other two. Okamoto-Barth and Call (2008) looked more closely at apes’ difficulty with rotations by testing whether adding persistent external landmark cues (e.g., different colored cups or an external marker on the correct cup) would help the apes’ performance. Indeed it did. With external cues, apes performed extremely well on rotations, even though landmarks alone were insufficient to tell them where the object was unless they explicitly saw the rotation. Of course, this begs the question of why these external landmarks made such a difference. One possibility is that the landmarks made it easier to track the movement of a particular object in the face of multiple moving objects. However, in that case, one must question whether this manipulation turned the task into a test of visible displacement rather than a true test of invisible displacement. Rooijakkers et al. (2009) compared all four ape species with dogs (described earlier) on a series of transpositions. Unlike dogs, all ape species scored extremely well, even on the transpositions in which containers crossed paths or an empty container moved into the original location of the baited container. Unfortunately, the experimenter looked at the containers during the apes’ choice, opening the possibility of unintentional social cues. Finally, Albiach-Serrano, Call, and Barth (2010) tested all four great ape species on 180-degree rotations. Both chimpanzees and bonobos passed, while gorillas and orangutans trended in the right direction but did not score significantly above chance. Unfortunately, there was no blinding procedure to guard against unintentional social cues.

Who Understands Invisible Displacement? The purpose of the current review was to critically examine studies of animal understanding of invisible displacement, in order to construct a coherent phylogenetic map of this ability across the animal kingdom. Table 4 summarizes the results of this exercise. When viewed through the lens of strict controls against sensory cues, social cues, and associative learning, we find that the map we are left with is threadbare indeed. It shows that great apes pass all three types of invisible displacement tasks, but beyond that, shows no clear positive evidence for invisible displacement understanding in any other animal species. Of course, the validity of this description relies on three methodological convictions which have not yet shared universal acceptance among researchers. Therefore, before discussing theoretical implications, it is worth revisiting these convictions.

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Table 4 Summary of Current Evidence Regarding Understanding Invisible Displacement in Different Animals Animal Birds

Piagetian task ?

Cats

Fail

Dogs

Fail

Dolphins Prosimians Monkeys Lesser apes Great apes

Fail Fail Fail ? Pass

Transposition Fail Pass simple lateral; Fail others Pass simple lateral; Fail others Fail ? ? ? Pass

Rotation Pass 90; Fail others ? Pass 90; Fail others ? ? ? ? Pass

Note. Understanding was coded as Pass if the animals passed the task in any studies with all the necessary controls, Fail if the animals failed the task in any studies, and? if no studies exist with all the necessary controls.

Do We Need Such Strict Blinding Requirements? Over the past 20 years, it has become evident that animal species exhibit profound differences in their ability to read and act on human social cues. For example, in hidden object tasks in which the correct location is intentionally cued by a human, dogs seem particularly skilled at deciphering cues such as pointing and gaze, whereas apes (other than human-raised apes) do not (e.g., Bräuer et al., 2006; Call & Tomasello, 2005; Miklósi et al., 1998). Given this, one might argue that for those animals who are not adept at such skills, a strict blinding requirement for invisible displacement tasks may be unnecessary, and should not disqualify what may otherwise be perfectly usable data. The problem is that this type of information is available only for certain animals and certain cues. For other animals (e.g., cats, birds), and for a variety of unintentional human cues (e.g., body tension, respiration changes, etc.), we simply don’t have the relevant data to make an accurate determination. Therefore, if we want to pursue a comparative understanding of invisible displacement, the obvious (and perhaps only) solution is to control for this issue across the board.6

Do We Need Such Strict Associative Learning Controls? Yes. Several studies have shown that animals who seem to pass the standard Piagetian invisible displacement task may do so by relying on associative learning, as shown by the fact that they fail these controls (e.g., Collier-Baker et al., 2004; Jaakkola et al., 2010; Neiworth et al., 2003). Therefore, a comprehensive set of such controls (i.e., employing both drop-first and drop-last procedures) is imperative for correctly characterizing the cognitive representations underlying animals’ performance. 6 I should note that if this requirement were dropped from the current review, the overall picture would change only in suggesting that African Grey parrots can pass the switch transposition task (Pepperberg et al., 1997). However, because we have no data regarding this species’ skill in reading human cues, it is impossible to know whether such an omission is acceptable.

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Do “Simpler” Transpositions and Rotations Reflect an Understanding of Invisible Displacement? Two studies have shown that dogs and cats are able to pass the very simplest transposition task in which the correct container does not cross paths with another container, and no other container moves into its original position (Doré et al., 1996; Rooijakkers et al., 2009). Similarly, three studies have shown that dogs and crows can pass the very simplest rotation task in which the baited container is positioned directly in front of the subject and is rotated 90-degrees to the right or left (Hoffman et al., 2011; Miller, Gipson et al., 2009; Miller, Rayburn-Reeves et al., 2009). But do these simpler tasks require an understanding of invisible displacement? I would argue that they do not. Rather, both can be solved by a straightforward attentional mechanism in which the animal’s attention is drawn to a single container, and it subsequently tracks that container. If its attention is temporarily diverted to another container (such as when containers cross paths or move into previously occupied locations as in the standard tasks), the animal is simply at a loss.

Theoretical Implications (And Why We Can’t Draw Them Yet) The current review has taken great pains to point out that apparent successes on experimental tasks with hidden objects may often be explained by a reliance on external cues rather than by a true understanding of invisible displacement. However, it is worth noting that similar cues often accompany hidden objects in the real world as well. That is, the vast majority of objects that move out of sight either (a) stay near the place where they went out of sight; (b) continue along their current trajectory; or (c) leave sensory cues (e.g., sounds, smells) regarding their changes in trajectory—all of which are trackable with an understanding of visible displacement, trajectory extrapolation, and sensory cues. And even in those rare cases in which hidden objects move with their containers/ occluders along a less predictable path (e.g., a baby marsupial in its mother’s pouch), such objects may be discoverable via associative learning (e.g., baby marsupials often go in and out of mothers’ pouches). Therefore, the relevant evolutionary issue may not be why a given animal has not evolved the ability to understand invisible displacement, but rather why any of them have. From a theoretical perspective, the question of animals’ understanding of invisible displacement is of particular importance due to its generally accepted status as an indicator of a powerful representational capacity—symbolic and/or secondary representation (Perner, 1991; Piaget, 1954; Suddendorf & Whiten, 2001). According to this view, the understanding of invisible displacement is one of a coherent cluster of abilities, including means-ends reasoning, mirror self-recognition, imitation, and understanding external representations, that accompanies the advent of secondary representation, whether developmentally in humans (Perner, 1991), or phylogenetically in the evolution of certain animal species (Suddendorf & Whiten, 2001). To understand the evolution of this type of cognitive representation, we must start with an accurate account of which

animals, with which ecological and evolutionary histories, show evidence of this ability. To the extent that this theoretical account is correct, the current analysis shows positive evidence for this type of representational capacity only in great apes (see also Suddendorf & Whiten, 2001). However, I would argue that the lack of sufficiently controlled studies makes it premature to conclude that this ability is necessarily lacking in other animal species. In particular, further research is warranted in at least three areas. First, several studies have suggested that certain birds—in particular, corvids and psittacids— demonstrate at least some abilities suggestive of a capacity for symbolic and/or secondary representation, including means-ends reasoning (Heinrich & Bugnyar, 2005; Weir, Chappell, & Kacelnik, 2002), symbol use (Pepperberg, 1999), and mirror self-recognition (Prior, Schwarz, & Güntürkün, 2008; but see Medina, Taylor, Hunt, & Gray, 2011). Therefore, we might also expect these birds to understand invisible displacement. Unfortunately, all standard Piagetian invisible displacement tasks with birds have either utilized the Uzgiris-Hunt procedure or have colocated a magnet with the target object. This leaves open a strong possibility of associative learning or direct perception of the object, leaving us with a gap in our knowledge of this ability in these birds. To fill this gap, we need straightforward studies of Piagetian invisible displacement, utilizing sensory controls, strict blinding, drop-first, and drop-last controls. Second, although bottlenose dolphins have been shown to fail invisible displacement tasks (Jaakkola et al., 2010), they have demonstrated strong abilities in almost every other area indicative of secondary representation, including imitation, mirror selfrecognition, means-ends reasoning, recognizing mental states, and understanding symbols and other external representations (for reviews, see Herman, 2006; Jaakkola, 2012; Jaakkola et al., 2010). Further research thus seems warranted to discover (a) whether dolphins’ ability to understand invisible displacement has been underestimated, or (b) why invisible displacement does not cluster with these related abilities in dolphins as it does in apes and human children. Finally, it is worth noting that all of the tasks in the current review utilize an active search response, which is arguably the most ecologically relevant measure of this type of knowledge. However, I would be remiss not to mention the growing number of studies showing that when tested with the more subtle measure of looking time to gauge violations of expectations, both monkeys and human infants show evidence of understanding properties of hidden objects that they do not show when measured with more traditional search tasks (e.g., Baillargeon, 1986, 1987; Baillargeon, Spelke, & Wasserman, 1985; Santos & Hauser, 2002; Santos, Seelig & Hauser, 2006). The reason for this discrepancy is still an active area of debate (e.g., Hood, Carey, & Prasada, 2000; Hood, Cole-Davies, & Dias, 2003; Mash, Novak, Berthier, & Keen, 2006; Santos et al., 2006). However, with respect to the current review, it is worth noting that these search-versus-looking-time discrepancies have all involved either (a) visible displacement tasks, or (b) a type of displacement in which the hidden movement is a continuation of the object’s trajectory before it disappeared from sight (i.e., a trajectory extrapolation. See Filion, Washburn, & Gulledge, 1996, for further evidence that monkeys can extrapolate trajectories). It is therefore still unknown whether animals and human infants would show evidence of understanding tradi-


tional invisible displacement (i.e., with containers that move in a manner not predictable by trajectory extrapolation) if tested in a violation of expectation paradigm.7


Conclusion In conclusion, I would like to acknowledge that the present review is both critical and conservative, by design. According to current theories, an important conceptual watershed separates the ability to understand visible displacement (which requires the use of a single mental model to represent the world faithfully) and the ability to understand invisible displacement (which requires the coordination of multiple mental models to represent how the world could be). A claim that an animal understands invisible displacement thus carries far-reaching conceptual implications, which necessitate a correspondingly high level of confidence in the data. The current review has shown that when we control for lower-level strategies, we can be confident that great apes have a conceptual understanding of invisible displacement. It may be that other nonhuman animals do as well, but the burden must be on us to show it.

7 The single study that has tested monkeys in a looking time version of a rotation task found that monkeys only passed when the hiding locations were nonidentical, suggesting that they solved the task by a method other than tracking the object’s hidden movement through the rotation (Hughes & Santos, 2012).

References Albiach-Serrano, A., Call, J., & Barth, J. (2010). Great apes track hidden objects after changes in the objects’ position and in subject’s orientation. American Journal of Primatology, 72, 349 –359. Anderson, M. R. (2012). Comprehension of object permanence and single transposition in gibbons. Behaviour, 149, 441– 459. doi:10.1163/ 156853912X639769 Auersperg, A. M. I., Szabo, B., von Bayern, A. M. P., & Bugnyar, T. (2013). Object permanence in the Goffin Cockatoo (Cacatua goffini). Journal of Comparative Psychology. Advance online publication. doi: 10.1037/a0033272 Baillargeon, R. (1986). Representing the existence and the location of hidden objects: Object permanence in 6- and 8-month-old infants. Cognition, 23, 21– 41. doi:10.1016/0010-0277(86)90052-1 Baillargeon, R. (1987). Object permanence in 3.5- and 4.5-month-old infants. Developmental Psychology, 23, 655– 664. doi:10.1037/00121649.23.5.655 Baillargeon, R., Spelke, E. S., & Wasserman, S. (1985). Object permanence in 5-month-old infants. Cognition, 20, 191–208. doi:10.1016/ 0010-0277(85)90008-3 Barth, J., & Call, J. (2006). Tracking the displacement of objects: A series of tasks with great apes (Pan troglodytes, Pan paniscus, Gorilla gorilla, and Pongo pygmaeus) and young children (Homo sapiens). Journal of Experimental Psychology: Animal Behavior Processes, 32, 239 –252. doi:10.1037/0097-7403.32.3.239 Beran, M. J., & Minahan, M. F. (2000). Monitoring spatial transpositions by bonobos (Pan paniscus) and chimpanzees (P. troglodytes). International Journal of Comparative Psychology, 13, 1–15. Bräuer, J., Kaminski, J., Riedel, J., Call, J., & Tomasello, M. (2006). Making inferences about the location of hidden food: Social dog, causal ape. Journal of Comparative Psychology, 120, 38 – 47. doi:10.1037/ 0735-7036.120.1.38

237

Bugnyar, T., Stöwe, M., & Heinrich, B. (2007). The ontogeny of caching in ravens, Corvus corax. Animal Behaviour, 74, 757–767. doi:10.1016/ j.anbehav.2006.08.019 Call, J. (2001). Object permanence in orangutans (Pongo pygmaeus), chimpanzees (Pan troglodytes), and children (Homo sapiens). Journal of Comparative Psychology, 115, 159 –171. doi:10.1037/0735-7036.115.2 .159 Call, J. (2003). Spatial rotations and transpositions in orangutans (Pongo pygmaeus) and chimpanzees (Pan troglodytes). Primates, 44, 347–357. doi:10.1007/s10329-003-0048-6 Call, J., & Tomasello, M. (2005). What chimpanzees know about seeing, revisited: An explanation of the third kind. In N. Eilan, C. Hoerl, T. McCormack, & J. Roessler (Eds.), Joint attention: Communication and other minds (pp. 45– 64). Oxford, UK: Oxford University Press. doi: 10.1093/acprof:oso/9780199245635.003.0003 Collier-Baker, E., Davis, J. M., Nielsen, M., & Suddendorf, T. (2006). Do chimpanzees (Pan troglodytes) understand single invisible displacement? Animal Cognition, 9, 55– 61. doi:10.1007/s10071-005-0004-5 Collier-Baker, E., Davis, J. M., & Suddendorf, T. (2004). Do dogs (Canis familiaris) understand invisible displacement? Journal of Comparative Psychology, 118, 421– 433. doi:10.1037/0735-7036.118.4.421 de Blois, S. T., & Novak, M. A. (1994). Object permanence in rhesus monkeys (Macaca mulatta). Journal of Comparative Psychology, 108, 318 –327. doi:10.1037/0735-7036.108.4.318 de Blois, S. T., Novak, M. A., & Bond, M. (1998). Object permanence in orangutans (Pongo pygmaeus) and squirrel monkeys (Saimiri sciureus). Journal of Comparative Psychology, 112, 137–152. doi:10.1037/07357036.112.2.137 Deppe, A. M., Wright, P. C., & Szelistowski, W. A. (2009). Object permanence in lemurs. Animal Cognition, 12, 381–388. doi:10.1007/ s10071-008-0197-5 Doré, F. Y. (1986). Object permanence in adult cats (Felis catus). Journal of Comparative Psychology, 100, 340 –347. doi:10.1037/0735-7036.100 .4.340 Doré, F. Y. (1990). Search behavior of cats (Felis catus) in an invisible displacement test: Cognition and experience. Canadian Journal of Psychology, 44, 359 –370. doi:10.1037/h0084262 Doré, F. Y., & Dumas, C. (1987). Psychology of animal cognition: Piagetian studies. Psychological Bulletin, 102, 219 –233. doi:10.1037/00332909.102.2.219 Doré, F. Y., Fiset, S., Goulet, S., Dumas, M. C., & Gagnon, S. (1996). Search behavior in cats and dogs: Interspecific differences in working memory and spatial cognition. Animal Learning & Behavior, 24, 142– 149. doi:10.3758/BF03198962 Doré, F. Y., & Goulet, S. (1998). The comparative analysis of object knowledge. In J. Langer & M. Killen (Eds.), Piaget, evolution and development (pp. 55–72). Mahwah, NJ: Erlbaum. Dumas, C. (1992). Object permanence in cats (Felis catus): An ecological approach to the study of invisible displacements. Journal of Comparative Psychology, 106, 404 – 410. doi:10.1037/0735-7036.106.4.404 Dumas, C., & Doré, F. Y. (1989). Cognitive development in kittens (Felis catus): A cross-sectional study of object permanence. Journal of Comparative Psychology, 103, 191–200. doi:10.1037/0735-7036.103.2.191 Fedor, A., Skollár, G., Szerencsy, N., & Ujhelyi, M. (2008). Object permanence tests on gibbons (Hylobatidae). Journal of Comparative Psychology, 122, 403– 417. doi:10.1037/0735-7036.122.4.403 Filion, C. M., Washburn, D. A., & Gulledge, J. P. (1996). Can monkeys (Macaca mulatta) represent invisible displacement? Journal of Comparative Psychology, 110, 386 –395. doi:10.1037/0735-7036.110.4.386 Fiset, S., & LeBlanc, V. (2007). Invisible displacement understanding in domestic dogs (Canis familiaris): The role of visual cues in search behavior. Animal Cognition, 10, 211–224. doi:10.1007/s10071-0060060-5


238

JAAKKOLA

Fiset, S., & Plourde, V. (2013). Object permanence in domestic dogs (Canis lupus familiaris) and gray wolves (Canis lupus). Journal of Comparative Psychology, 127, 115–127. doi:10.1037/a0030595 Funk, M. S. (1996). Development of object permanence in the New Zealand parakeet (Cyanoramphus auriceps). Animal Learning & Behavior, 24, 375–383. doi:10.3758/BF03199009 Furlong, E. E., Boose, K. J., & Boysen, S. T. (2008). Raking it in: The impact of enculturation on chimpanzee tool use. Animal Cognition, 11, 83–97. doi:10.1007/s10071-007-0091-6 Gagnon, S., & Doré, F. Y. (1992). Search behavior in various breeds of adult dogs (Canis familiaris): Object permanence and olfactory cues. Journal of Comparative Psychology, 106, 58 – 68. doi:10.1037/07357036.106.1.58 Gagnon, S., & Doré, F. Y. (1993). Search behavior of dogs (Canis familiaris) in invisible displacement problems. Animal Learning & Behavior, 21, 246 –254. doi:10.3758/BF03197989 Goodenough, J., McGuire, B., & Jakob, E. (2010). Perspectives on animal behavior. New York, NY: Wiley. Goulet, S., Doré, F. Y., & Rousseau, R. (1994). Object permanence and working memory in cats (Felis catus). Journal of Experimental Psychology: Animal Behavior Processes, 20, 347–365. doi:10.1037/0097-7403 .20.4.347 Harris, P. L. (1987). The development of search. In P. Salapatek & L. B. Gohen (Eds.), Handbook of infant perception (Vol. 2, pp. 155–207). New York, NY: Academic Press. Heinrich, B., & Bugnyar, T. (2005). Testing problem solving in ravens: String-pulling to reach food. Ethology, 111, 962–976. doi:10.1111/j .1439-0310.2005.01133.x Herman, L. M. (2006). Intelligence and rational behaviour in the bottlenosed dolphin. In S. Hurley & M. Nudds (Eds.), Rational animals? (pp. 439 – 467). Oxford, UK: Oxford University Press. doi:10.1093/acprof: oso/9780198528272.003.0020 Hoffmann, A., Rüttler, V., & Nieder, A. (2011). Ontogeny of object permanence and object tracking in the carrion crow (Corvus corone). Animal Behaviour, 82, 359 –367. doi:10.1016/j.anbehav.2011.05.012 Hood, B., Carey, S., & Prasada, S. (2000). Predicting the outcomes of physical events: Two-year-olds fail to reveal knowledge of solidity and support. Child Development, 71, 1540 –1554. doi:10.1111/1467-8624 .00247 Hood, B., Cole-Davies, V., & Dias, M. (2003). Looking and search measures of object knowledge in preschool children. Developmental Psychology, 39, 61–70. doi:10.1037/0012-1649.39.1.61 Hughes, K. D., & Santos, L. R. (2012). Rotational displacement skills in rhesus macaques (Macaca mulatta). Journal of Comparative Psychology, 126, 421– 432. doi:10.1037/a0028757 Jaakkola, K. (2012). Cetacean cognitive specializations. In J. Vonk & T. Shackleford (Eds.), The Oxford handbook of comparative evolutionary psychology (pp. 671– 688). New York, NY: Oxford University Press. doi:10.1093/oxfordhb/9780199738182.013.0009 Jaakkola, K., Guarino, E., Rodriguez, M., Erb, L., & Trone, M. (2010). What do dolphins (Tursiops truncatus) understand about hidden objects? Animal Cognition, 13, 103–120. doi:10.1007/s10071-009-0250-z Mallavarapu, S., Perdue, B. M., Stoinski, T. S., & Maple, T. L. (2013). Can black-and-white ruffed lemurs (Varecia variegata) solve object permanence tasks? American Journal of Primatology, 75, 376 –386. doi: 10.1002/ajp.22118 Marcovitch, S., & Zelazo, P. D. (1999). The A-not-B error: Results from a logistic meta-analysis. Child Development, 70, 1297–1313. doi: 10.1111/1467-8624.00095 Mash, C., Novak, E., Berthier, N. E., & Keen, R. (2006). What do two-year-olds understand about hidden-object events? Developmental Psychology, 42, 263–271. doi:10.1037/0012-1649.42.2.263 Mathieu, M., Bouchard, M. A., Granger, L., & Herscovitch, J. (1976). Piagetian object permanence in Cebus capucinus, Lagothrica flavicauda

and Pan troglodytes. Animal Behaviour, 24, 585–588. doi:10.1016/ S0003-3472(76)80071-1 Medina, F. S., Taylor, A. H., Hunt, G. R., & Gray, R. D. (2011). New Caledonian crows’ responses to mirrors. Animal Behaviour, 82, 981– 993. doi:10.1016/j.anbehav.2011.07.033 Mendes, N., & Huber, L. (2004). Object permanence in common marmosets (Callithrix jacchus). Journal of Comparative Psychology, 118, 103–112. doi:10.1037/0735-7036.118.1.103 Miklósi, Á., Polgárdi, R., Topál, J., & Csányi, V. (1998). Use of experimenter-given cues in dogs. Animal Cognition, 1, 113–121. doi: 10.1007/s100710050016 Miklósi, A., & Soproni, K. (2006). A comparative analysis of animals’ understanding of the human pointing gesture. Animal Cognition, 9, 81–93. doi:10.1007/s10071-005-0008-1 Miller, H. C., Gipson, C. D., Vaughan, A., Rayburn-Reeves, R., & Zentall, T. R. (2009). Object permanence in dogs: Invisible displacement in a rotation task. Psychonomic Bulletin & Review, 16, 150 –155. doi: 10.3758/PBR.16.1.150 Miller, H. C., Rayburn-Reeves, R., & Zentall, T. R. (2009). What do dogs know about hidden objects? Behavioural Processes, 81, 439 – 446. doi: 10.1016/j.beproc.2009.03.018 Natale, F., Antinucci, F., Spinozzi, G., & Potì, P. (1986). Stage 6 object concept in nonhuman primate cognition: A comparison between gorilla (Gorilla gorilla gorilla) and Japanese macaque (Macaca fuscata). Journal of Comparative Psychology, 100, 335–339. doi:10.1037/0735-7036 .100.4.335 Neiworth, J. J., Steinmark, E., Basile, B. M., Wonders, R., Steely, F., & DeHart, C. (2003). A test of object permanence in a new-world monkey species, cotton top tamarins (Saguinus oedipus). Animal Cognition, 6, 27–37. doi:10.1007/s10071-003-0162-2 Okamoto-Barth, S., & Call, J. (2008). Tracking and inferring spatial rotation by children and great apes. Developmental Psychology, 44, 1396 –1408. doi:10.1037/a0012594 Pasnak, R., Kurkjian, M., & Triana, E. (1988). Assessment of stage 6 object permanence. Bulletin of the Psychonomic Society, 26, 368 –370. doi:10.3758/BF03337685 Pepperberg, I. M. (1999). The Alex studies: Cognitive and communicative abilities of Grey parrots. Cambridge, MA: Harvard University Press. Pepperberg, I. M. (2002). The value of the Piagetian framework for comparative cognitive studies. Animal Cognition, 5, 177–182. doi: 10.1007/s10071-002-0148-5 Pepperberg, I. M., & Funk, M. S. (1990). Object permanence in four species of psittacine birds: An African Grey parrot (Psittacus erithacus), an Illiger mini macaw (Ara maracana), a parakeet (Melopsittacus undulatus) and a cockatiel (Nymphicus hollandicus). Animal Learning & Behavior, 18, 97–108. doi:10.3758/BF03205244 Pepperberg, I. M., & Kozak, F. A. (1986). Object permanence in the African Grey parrot (Psittacus erithacus). Animal Learning & Behavior, 14, 322–330. doi:10.3758/BF03200074 Pepperberg, I. M., Willner, M. R., & Gravitz, L. B. (1997). Development of Piagetian object permanence in a Grey parrot (Psittacus erithacus). Journal of Comparative Psychology, 111, 63–75. doi:10.1037/07357036.111.1.63 Perner, J. (1991). Understanding the representational mind. Cambridge, MA: MIT Press. Pfungst, O. (1911). Clever Hans (The horse of Mr. Van Osten): A contribution to experimental animal and human psychology. New York, NY: Henry Holt and Company. doi:10.5962/bhl.title.56164 Piaget, J. (1954). The construction of reality in the child. New York, NY: Basic Books. doi:10.1037/11168-000 Pollok, B., Prior, H., & Güntürkün, O. (2000). Development of object permanence in food-storing magpies (Pica pica). Journal of Comparative Psychology, 114, 148 –157. doi:10.1037/0735-7036.114.2.148


DO ANIMALS UNDERSTAND INVISIBLE DISPLACEMENT? Prior, H., Schwarz, A., & Güntürkün, O. (2008). Mirror-induced behavior in the magpie (Pica pica): Evidence of self-recognition. PLOS Biology, 6, e202. doi:10.1371/journal.pbio.0060202 Redshaw, M. (1978). Cognitive development in human and gorilla infants. Journal of Human Evolution, 7, 133–141. doi:10.1016/S00472484(78)80005-0 Rooijakkers, E. F., Kaminski, J., & Call, J. (2009). Comparing dogs and great apes in their ability to visually track object transpositions. Animal Cognition, 12, 789 –796. doi:10.1007/s10071-009-0238-8 Santos, L. R., & Hauser, M. D. (2002). A non-human primate’s understanding of solidity: Dissociations between seeing and acting. Developmental Science, 5, F1–F7. doi:10.1111/1467-7687.t01-1-00216 Santos, L. R., Seelig, D., & Hauser, M. D. (2006). Cotton-top tamarins’ (Saguinus oedipus) expectations about occluded objects: A dissociation between looking and reaching tasks. Infancy, 9, 147–171. doi:10.1207/ s15327078in0902_4 Schino, G., Spinozzi, G., & Berlinguer, L. (1990). Object concept and mental representation in Cebus apella and Macaca fascicularis. Primates, 31, 537–544. doi:10.1007/BF02382536 Sophian, C., & Sage, S. (1983). Developments in infants’ search for displaced objects. Journal of Experimental Child Psychology, 35, 143– 160. doi:10.1016/0022-0965(83)90075-9 Suddendorf, T., & Whiten, A. (2001). Mental evolution and development: Evidence for secondary representation in children, great apes, and other animals. Psychological Bulletin, 127, 629 – 650. doi:10.1037/0033-2909 .127.5.629 Tomasello, M., & Call, J. (1997). Primate cognition. New York, NY: Oxford University Press. Tomasello, M., & Call, J. (2004). The role of humans in the cognitive development of apes revisited. Animal Cognition, 7, 213–215. doi: 10.1007/s10071-004-0227-x

239

Triana, E., & Pasnak, R. (1981). Object permanence in cats and dogs. Animal Learning & Behavior, 9, 135–139. doi:10.3758/BF03212035 Ujfalussy, D. J., Miklósi, A., & Bugnyar, T. (2013). Ontogeny of object permanence in a non-storing corvid species, the jackdaw (Corvus monedula). Animal Cognition, 16, 405– 416. doi:10.1007/s10071-0120581-z Uzgiris, I. C., & Hunt, J. M. (1975). Assessment in infancy: Ordinal scales of psychological development. Champaign-Urbana, IL: University of Illinois Press. van Schaik, C. P., & Burkart, J. M. (2011). Social learning and evolution: The cultural intelligence hypothesis. Philosophical Transactions of the Royal Society B, 366, 1008 –1016. doi:10.1098/rstb.2010.0304 Weir, A. A. S., Chappell, J., & Kacelnik, A. (2002). Shaping of hooks in New Caledonian crows. Science, 297, 981. doi:10.1126/science.1073433 Wiltschko, R., & Wiltschko, W. (2006). Magnetoreception. BioEssays, 28, 157–168. doi:10.1002/bies.20363 Wise, K. L., Wise, L. A., & Zimmerman, R. R. (1974). Piagetian object permanence in the infant rhesus monkey. Developmental Psychology, 10, 429 – 437. doi:10.1037/h0036405 Wood, S., Moriarty, K. M., Gardner, B. T., & Gardner, R. A. (1980). Object permanence in child and chimpanzee. Animal Learning & Behavior, 8, 3–9. doi:10.3758/BF03209723 Zucca, P., Milos, N., & Vallortigara, G. (2007). Piagetian object permanence and its development in Eurasian jays (Garrulus glandarius). Animal Cognition, 10, 243–258. doi:10.1007/s10071-006-0063-2

Received June 14, 2013 Revision received December 11, 2013 Accepted December 11, 2013 䡲

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