Beyond the Tricks: The Science and Comparative Cognition of Magic.

Magic is an art form that has fascinated humans for centuries. Recently, the techniques used by magicians to make their audience experience the impossible have attracted the attention of psychologists, who, in just a couple of decades, have produced a large amount of research regarding how these effects operate, focusing on the blind spots in perception and roadblocks in cognition that magic techniques exploit. Most recently, this investigation has given a pathway to a new line of research that uses magic effects to explore the cognitive abilities of nonhuman animals. This new branch of the scientific study of magic has already yielded new evidence illustrating the power of magic effects as a psychological tool for nonhuman animals. This review aims to give a thorough overview of the research on both the human and nonhuman perception of magic effects by critically illustrating the most prominent works of both fields of inquiry.

Exploring the perceptual inabilities of Eurasian jays (Garrulus glandarius) using magic effects.

In recent years, scientists have begun to use magic effects to investigate the blind spots in our attention and perception [G. Kuhn, Experiencing the Impossible: The Science of Magic (2019); S. Macknik, S. Martinez-Conde, S. Blakeslee, Sleights of Mind: What the Neuroscience of Magic Reveals about Our Everyday Deceptions (2010)]. Recently, we suggested that similar techniques could be transferred to nonhuman animal observers and that such an endeavor would provide insight into the inherent commonalities and discrepancies in attention and perception in human and nonhuman animals [E. Garcia-Pelegrin, A. K. Schnell, C. Wilkins, N. S. Clayton, Science 369, 1424-1426 (2020)]. Here, we performed three different magic effects (palming, French drop, and fast pass) to a sample of six Eurasian jays (Garrulus glandarius). These magic effects were specifically chosen as they utilize different cues and expectations that mislead the spectator into thinking one object has or has not been transferred from one hand to the other. Results from palming and French drop experiments suggest that Eurasian jays have different expectations from humans when observing some of these effects. Specifically, Eurasian jays were not deceived by effects that required them to expect an object to move between hands when observing human hand manipulations. However, similar to humans, Eurasian jays were misled by magic effects that utilize fast movements as a deceptive action. This study investigates how another taxon perceives the magician's techniques of deception that commonly deceive humans.

Mirror-mediated string-pulling task in Eurasian jays (Garrulus glandarius).

Mirror tasks can be used to investigate whether animals can instrumentally use a mirror to solve problems and can understand the correspondence between reflections and the real objects they represent. Two bird species, a corvid (New Caledonian crow) and a parrot (African grey parrot), have demonstrated the ability to use mirrors instrumentally in mirror-mediated spatial locating tasks. However, they have not been challenged with a mirror-guided reaching task, which involves a more complex understanding of the mirror's properties. In the present study, a task approximating the mirror-guided reaching task used in primate studies was adapted for, and given to, a corvid species (Eurasian jay) using a horizontal string-pulling paradigm. Four birds learned to pull the correct string to retrieve a food reward when they could see the food directly, whereas none used the reflected information to accomplish the same objective. Based on these results, it cannot be concluded whether these birds understand the correspondence between the location of the reward and its reflected information, or if the relative lack of visual-perceptual motor feedback given by the setup interfered with their performance. This novel task is posited to be conceptually more difficult compared to mirror-mediated spatial locating tasks, and should be used in avian species that have previously been successful at using the mirror instrumentally. This would establish whether these species can still succeed at it, and thus whether the task does indeed pose additional cognitive demands.

Elephants have a nose for quantity.

Animals often face situations that require making decisions based on quantity. Many species, including humans, rely on an ability to differentiate between more and less to make judgments about social relationships, territories, and food. Habitat-related choices require animals to decide between areas with greater and lesser quantities of food while also weighing relative risk of danger based on group size and predation risk. Such decisions can have a significant impact on survival for an animal and its social group. Many species have demonstrated a capacity for differentiating between two quantities of food and choosing the greater of the two, but they have done so based on information provided primarily in the visual domain. Using an object-choice task, we demonstrate that elephants are able to discriminate between two distinct quantities using their olfactory sense alone. We presented the elephants with choices between two containers of sunflower seeds. The relationship between the amount of seeds within the two containers was represented by 11 different ratios. Overall, the elephants chose the larger quantity of food by smelling for it. The elephants' performance was better when the relative difference between the quantities increased and worse when the ratio between the quantities of food increased, but was not affected by the overall quantity of food presented. These results are consistent with the performance of animals tested in the visual domain. This work has implications for the design of future, cross-phylogenetic cognitive comparisons that ought to account for differences in how animals sense their world.

Cephalopods: Ambassadors for rethinking cognition.

Traditional approaches in comparative cognition have a long history of focusing on a narrow range of vertebrate species. However, in recent years the range of model species has expanded. Despite this development, invertebrate taxa are still largely neglected in comparative cognition, which limits our ability to locate the origins of cognitive traits. The time has come to rethink cognition and develop a more comprehensive understanding of cognitive evolution by expanding comparative analyses to include a diverse range of invertebrate taxa. In this review, we contend that cephalopods are suitable ambassadors for rethinking cognition. Cephalopods have large complex brains, exhibit sophisticated behavioral traits, and increasing evidence suggests that they possess complex cognitive abilities once thought to be unique to large-brained vertebrates. Comparing cephalopods with vertebrates, whose cognition has evolved independently, provides prominent opportunities to circumvent current limitations in comparative cognition that have arisen from traditional vertebrate comparisons. Increased efforts in investigating the cognitive abilities of cephalopods have also led to important welfare-related improvements. These large-brained molluscs are paving the way for a more inclusive approach to investigating cognitive evolution that we hope will extend to other invertebrate taxa.

Episodic-like memory is preserved with age in cuttlefish.

Episodic memory, remembering past experiences based on unique what-where-when components, declines during ageing in humans, as does episodic-like memory in non-human mammals. By contrast, semantic memory, remembering learnt knowledge without recalling unique what-where-when features, remains relatively intact with advancing age. The age-related decline in episodic memory likely stems from the deteriorating function of the hippocampus in the brain. Whether episodic memory can deteriorate with age in species that lack a hippocampus is unknown. Cuttlefish are molluscs that lack a hippocampus. We test both semantic-like and episodic-like memory in sub-adults and aged-adults nearing senescence (n = 6 per cohort). In the semantic-like memory task, cuttlefish had to learn that the location of a food resource was dependent on the time of day. Performance, measured as proportion of correct trials, was comparable across age groups. In the episodic-like memory task, cuttlefish had to solve a foraging task by retrieving what-where-when information about a past event with unique spatio-temporal features. In this task, performance was comparable across age groups; however, aged-adults reached the success criterion (8/10 correct choices in consecutive trials) significantly faster than sub-adults. Contrary to other animals, episodic-like memory is preserved in aged cuttlefish, suggesting that memory deterioration is delayed in this species.

Cuttlefish exert self-control in a delay of gratification task.

The ability to exert self-control varies within and across taxa. Some species can exert self-control for several seconds whereas others, such as large-brained vertebrates, can tolerate delays of up to several minutes. Advanced self-control has been linked to better performance in cognitive tasks and has been hypothesized to evolve in response to specific socio-ecological pressures. These pressures are difficult to uncouple because previously studied species face similar socio-ecological challenges. Here, we investigate self-control and learning performance in cuttlefish, an invertebrate that is thought to have evolved under partially different pressures to previously studied vertebrates. To test self-control, cuttlefish were presented with a delay maintenance task, which measures an individual's ability to forgo immediate gratification and sustain a delay for a better but delayed reward. Cuttlefish maintained delay durations for up to 50-130 s. To test learning performance, we used a reversal-learning task, whereby cuttlefish were required to learn to associate the reward with one of two stimuli and then subsequently learn to associate the reward with the alternative stimulus. Cuttlefish that delayed gratification for longer had better learning performance. Our results demonstrate that cuttlefish can tolerate delays to obtain food of higher quality comparable to that of some large-brained vertebrates.

Convergent evolution of complex cognition: Insights from the field of avian cognition into the study of self-awareness.

Pioneering research on avian behaviour and cognitive neuroscience have highlighted that avian species, mainly corvids and parrots, have a cognitive tool kit comparable with apes and other large-brained mammals, despite conspicuous differences in their neuroarchitecture. This cognitive tool kit is driven by convergent evolution, and consists of complex processes such as casual reasoning, behavioural flexibility, imagination, and prospection. Here, we review experimental studies in corvids and parrots that tested complex cognitive processes within this tool kit. We then provide experimental examples for the potential involvement of metacognitive skills in the expression of the cognitive tool kit. We further expand the discussion of cognitive and metacognitive abilities in avian species, suggesting that an integrated assessment of these processes, together with revised and multiple tasks of mirror self-recognition, might shed light on one of the most highly debated topics in the literature-self-awareness in animals. Comparing the use of multiple assessments of self-awareness within species and across taxa will provide a more informative, richer picture of the level of consciousness in different organisms.

Delayed gratification in New Caledonian crows and young children: influence of reward type and visibility.

Self-control underlies cognitive abilities such as decision making and future planning. Delay of gratification is a measure of self-control and involves obtaining a more valuable outcome in the future by tolerating a delay or investing a greater effort in the present. Contextual issues, such as reward visibility and type, may influence delayed gratification performance, although there has been limited comparative investigation between humans and other animals, particularly non-primate species. Here, we adapted an automated 'rotating tray' paradigm used previously with capuchin monkeys to test for delay of gratification ability that requires little pre-test training, where the subject must forgo an immediate, less preferred reward for a delayed, more preferred one. We tested New Caledonian crows and 3-5-year-old human children. We manipulated reward types to differ in quality or quantity (Experiments 1 and 2) as well as visibility (Experiment 2). In Experiments 1 and 2, both species performed better when the rewards varied in quality as opposed to quantity, though performed above chance in both conditions. In Experiment 1, both crows and children were able to delay gratification when both rewards were visible. In Experiment 2, 5-year-old children outperformed 3- and 4-year olds, though overall children still performed well, while the crows struggled when reward visibility was manipulated, a result which may relate to difficulties in tracking the experimenters' hands during baiting. We discuss these findings in relation to the role of contextual issues on self-control when making species comparisons and investigating the mechanisms of self-control.

Cuttlefish show flexible and future-dependent foraging cognition.

Some animals optimize their foraging activity by learning and memorizing food availability, in terms of quantity and quality, and adapt their feeding behaviour accordingly. Here, we investigated whether cuttlefish flexibly adapt their foraging behaviour according to the availability of their preferred prey. In Experiment 1, cuttlefish switched from a selective to an opportunistic foraging strategy (or vice versa) when the availability of their preferred prey at night was predictable versus unpredictable. In Experiment 2, cuttlefish exhibited day-to-day foraging flexibility, in response to experiencing changes in the proximate future (i.e. preferred prey available on alternate nights). In Experiment 1, the number of crabs eaten during the day decreased when shrimp (i.e. preferred food) were predictably available at night, while the consumption of crabs during the day was maintained when shrimp availability was unpredictable. Cuttlefish quickly shifted from one strategy to the other, when experimental conditions were reversed. In Experiment 2, cuttlefish only reduced their consumption of crabs during the daytime when shrimps were predictably available the following night. Their daytime foraging behaviour appeared dependent on shrimps' future availability. Overall, cuttlefish can adopt dynamic and flexible foraging behaviours including selective, opportunistic and future-dependent strategies, in response to changing foraging conditions.

New Caledonian crows infer the weight of objects from observing their movements in a breeze.

Humans use a variety of cues to infer an object's weight, including how easily objects can be moved. For example, if we observe an object being blown down the street by the wind, we can infer that it is light. Here, we tested whether New Caledonian crows make this type of inference. After training that only one type of object (either light or heavy) was rewarded when dropped into a food dispenser, birds observed pairs of novel objects (one light and one heavy) suspended from strings in front of an electric fan. The fan was either on-creating a breeze which buffeted the light, but not the heavy, object-or off, leaving both objects stationary. In subsequent test trials, birds could drop one, or both, of the novel objects into the food dispenser. Despite having no opportunity to handle these objects prior to testing, birds touched the correct object (light or heavy) first in 73% of experimental trials, and were at chance in control trials. Our results suggest that birds used pre-existing knowledge about the behaviour exhibited by differently weighted objects in the wind to infer their weight, using this information to guide their choices.

Comparing the face inversion effect in crows and humans.

Humans show impaired recognition of faces that are presented upside down, a phenomenon termed face inversion effect, which is thought to reflect the special relevance of faces for humans. Here, we investigated whether a phylogenetically distantly related avian species, the carrion crow, with similar socio-cognitive abilities to human and non-human primates, exhibits a face inversion effect. In a delayed matching-to-sample task, two crows had to differentiate profiles of crow faces as well as matched controls, presented both upright and inverted. Because crows can discriminate humans based on their faces, we also assessed the face inversion effect using human faces. Both crows performed better with crow faces than with human faces and performed worse when responding to inverted pictures in general compared to upright pictures. However, neither of the crows showed a face inversion effect. For comparative reasons, the tests were repeated with human subjects. As expected, humans showed a face-specific inversion effect. Therefore, we did not find any evidence that crows-like humans-process faces as a special visual stimulus. Instead, individual recognition in crows may be based on cues other than a conspecific's facial profile, such as their body, or on processing of local features rather than holistic processing.

California scrub-jays reduce visual cues available to potential pilferers by matching food colour to caching substrate.

Some animals hide food to consume later; however, these caches are susceptible to theft by conspecifics and heterospecifics. Caching animals can use protective strategies to minimize sensory cues available to potential pilferers, such as caching in shaded areas and in quiet substrate. Background matching (where object patterning matches the visual background) is commonly seen in prey animals to reduce conspicuousness, and caching animals may also use this tactic to hide caches, for example, by hiding coloured food in a similar coloured substrate. We tested whether California scrub-jays (Aphelocoma californica) camouflage their food in this way by offering them caching substrates that either matched or did not match the colour of food available for caching. We also determined whether this caching behaviour was sensitive to social context by allowing the birds to cache when a conspecific potential pilferer could be both heard and seen (acoustic and visual cues present), or unseen (acoustic cues only). When caching events could be both heard and seen by a potential pilferer, birds cached randomly in matching and non-matching substrates. However, they preferentially hid food in the substrate that matched the food colour when only acoustic cues were present. This is a novel cache protection strategy that also appears to be sensitive to social context. We conclude that studies of cache protection strategies should consider the perceptual capabilities of the cacher and potential pilferers.

Evolution of iris colour in relation to cavity nesting and parental care in passerine birds.

Strong selection pressures are known to act on animal coloration. Although many animals vary in eye colour, virtually no research has investigated the functional significance of these colour traits. Passeriformes have a range of iris colours, making them an ideal system to investigate how and why iris colour has evolved. Using phylogenetic comparative methods, we tested the hypothesis that conspicuous iris colour in passerine birds evolved in response to (a) coordination of offspring care and (b) cavity nesting, two traits thought to be involved in intra-specific gaze sensitivity. We found that iris colour and cooperative offspring care by two or more individuals evolved independently, suggesting that bright eyes are not important for coordinating parental care through eye gaze. Furthermore, we found that evolution between iris colour and nesting behaviour did occur in a dependent manner, but contrary to predictions, transitions to coloured eyes were not more frequent in cavity nesters than non-cavity nesters. Instead, our results indicate that selection away from having bright eyes was much stronger in non-cavity nesters than cavity nesters, perhaps because conspicuous eye coloration in species not concealed within a cavity would be more visible to predators.

Wild jackdaws' reproductive success and their offspring's stress hormones are connected to provisioning rate and brood size, not to parental neophobia.

Many species show individual variation in neophobia and stress hormones, but the causes and consequences of this variation in the wild are unclear. Variation in neophobia levels could affect the number of offspring animals produce, and more subtly influence the rearing environment and offspring development. Nutritional deficits during development can elevate levels of stress hormones that trigger long-term effects on learning, memory, and survival. Therefore measuring offspring stress hormone levels, such as corticosterone (CORT), helps determine if parental neophobia influences the condition and developmental trajectory of young. As a highly neophobic species, jackdaws (Corvus monedula) are excellent for exploring the potential effects of parental neophobia on developing offspring. We investigated if neophobic responses, alongside known drivers of fitness, influence nest success and offspring hormone responses in wild breeding jackdaws. Despite its consistency across the breeding season, and suggestions in the literature that it should have importance for reproductive fitness, parental neophobia did not predict nest success, provisioning rates or offspring hormone levels. Instead, sibling competition and poor parental care contributed to natural variation in stress responses. Parents with lower provisioning rates fledged fewer chicks, chicks from larger broods had elevated baseline CORT levels, and chicks with later hatching dates showed higher stress-induced CORT levels. Since CORT levels may influence the expression of adult neophobia, variation in juvenile stress responses could explain the development and maintenance of neophobic variation within the adult population.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Hint-seeking behaviour of western scrub-jays in a metacognition task.

Metacognitive processes during memory retrieval can be tested by examining whether or not animals can assess their knowledge state when they are faced with a memory test. In a typical foraging task, food is hidden in one of the multiple tubes and the subjects are given an opportunity to check the contents of the tubes before choosing the one that they thought contained food. Following the findings from our previous study that western scrub-jays (Aphelocoma californica) can make prospective metacognition judgements, this study tested the scrub-jays' concurrent metacognition judgements. In a series of experiments, uncertainty about the food location was induced in three ways: by making the baiting process visibly unavailable, by inserting a delay between the baiting and food retrieval, and by moving the location of the bait. The jays looked into the tubes more often during the conditions that were consistent with high uncertainty. In addition, their looking behaviour was associated not with the sight of food but with information about the location of the food. These findings suggest that the jays can differentiate the states of knowing and not knowing about certain information and take appropriate action to complement their missing knowledge.

Caching at a distance: a cache protection strategy in Eurasian jays.

A fundamental question about the complexity of corvid social cognition is whether behaviours exhibited when caching in front of potential pilferers represent specific attempts to prevent cache loss (cache protection hypothesis) or whether they are by-products of other behaviours (by-product hypothesis). Here, we demonstrate that Eurasian jays preferentially cache at a distance when observed by conspecifics. This preference for a 'far' location could be either a by-product of a general preference for caching at that specific location regardless of the risk of cache loss or a by-product of a general preference to be far away from conspecifics due to low intra-species tolerance. Critically, we found that neither by-product account explains the jays' behaviour: the preference for the 'far' location was not shown when caching in private or when eating in front of a conspecific. In line with the cache protection hypothesis we found that jays preferred the distant location only when caching in front of a conspecific. Thus, it seems likely that for Eurasian jays, caching at a distance from an observer is a specific cache protection strategy.

An avian perspective on simulating other minds.

An exciting new study on ravens by Bugnyar, Reber, and Buckner (2016) raises important questions about whether nonhuman animals are capable of simulating other minds, rather than theorizing about them.

New perspectives in gaze sensitivity research.

Attending to where others are looking is thought to be of great adaptive benefit for animals when avoiding predators and interacting with group members. Many animals have been reported to respond to the gaze of others, by co-orienting their gaze with group members (gaze following) and/or responding fearfully to the gaze of predators or competitors (i.e., gaze aversion). Much of the literature has focused on the cognitive underpinnings of gaze sensitivity, namely whether animals have an understanding of the attention and visual perspectives in others. Yet there remain several unanswered questions regarding how animals learn to follow or avoid gaze and how experience may influence their behavioral responses. Many studies on the ontogeny of gaze sensitivity have shed light on how and when gaze abilities emerge and change across development, indicating the necessity to explore gaze sensitivity when animals are exposed to additional information from their environment as adults. Gaze aversion may be dependent upon experience and proximity to different predator types, other cues of predation risk, and the salience of gaze cues. Gaze following in the context of information transfer within social groups may also be dependent upon experience with group-members; therefore we propose novel means to explore the degree to which animals respond to gaze in a flexible manner, namely by inhibiting or enhancing gaze following responses. We hope this review will stimulate gaze sensitivity research to expand beyond the narrow scope of investigating underlying cognitive mechanisms, and to explore how gaze cues may function to communicate information other than attention.