Yes, dogs are susceptible to the Kanizsa's triangle illusion: A reply to Pepperberg.

A recent paper by Pepperberg, Learning & Behavior, 51, 5-6, (2023) enquires about the validity of the finding that dogs are susceptible to the Kanizsa's triangle illusion, reported by Lõoke and coauthors (Lõoke et al., Animal Cognition, 25, 43-51, 2022). Here we elaborate on the matter, providing both theoretical considerations and further data, supporting the soundness of our previous conclusions.

Quantitative abilities of invertebrates: a methodological review.

Quantitative abilities are widely recognized to play important roles in several ecological contexts, such as foraging, mate choice, and social interaction. Indeed, such abilities are widespread among vertebrates, in particular mammals, birds, and fish. Recently, there has been an increasing number of studies on the quantitative abilities of invertebrates. In this review, we present the current knowledge in this field, especially focusing on the ecological relevance of the capacity to process quantitative information, the similarities with vertebrates, and the different methods adopted to investigate this cognitive skill. The literature argues, beyond methodological differences, a substantial similarity between the quantitative abilities of invertebrates and those of vertebrates, supporting the idea that similar ecological pressures may determine the emergence of similar cognitive systems even in distantly related species.

Dogs (Canis lupus familiaris) are susceptible to the Kanizsa's triangle illusion.

The ability to complete partially missing contours is widespread across the animal kingdom, but whether this extends to dogs is still unknown. To address this gap in knowledge, we assessed dogs' susceptibility to one of the most common contour illusions, the Kanizsa's triangle. Six dogs were trained to discriminate a triangle from other geometrical figures using a two-alternative conditioned discrimination task. Once the learning criterion was reached, dogs were presented with the Kanizsa's triangle and a control stimulus, where inducers were rotated around their centre, so as to disrupt what would be perceived as a triangle by a human observer. As a group, dogs chose the illusory triangle significantly more often than control stimuli. At the individual level, susceptibility to the illusion was shown by five out of six dogs. This is the first study where dogs as a group show susceptibility to a visual illusion in the same manner as humans. Moreover, the analyses revealed a negative effect of age on susceptibility, an effect that was also found in humans. Altogether, this suggests that the underling perceptual mechanisms are similar between dogs and humans, and in sharp contrast with other categories of visual illusions to which the susceptibility of dogs has been previously assessed.

Guppies (Poecilia reticulata) are deceived by visual illusions during obstacle negotiation.

Animals travelling in their natural environment repeatedly encounter obstacles that they can either detour or go through. Gap negotiation requires an accurate estimation of the opening's size to avoid getting stuck or being injured. Research on visual illusions has revealed that in some circumstances, transformation rules used to generate a three-dimensional representation from bidimensional retinal images fail, leading to systematic errors in perception. In Ebbinghaus and Delboeuf illusions, the presence of task-irrelevant elements causes us to misjudge an object's size. Susceptibility to these illusions was observed in other animals, although with large intraspecific differences. In this study, we investigated whether fish can accurately estimate gap size and whether during this process they may be deceived by illusory patterns. Guppies were extremely accurate in gap negotiation, discriminating holes with a 10% diameter difference. When presented with two identical holes surrounded by inducers to produce Ebbinghaus and Delboeuf patterns, guppies misperceived gap size in the predicted direction. So far, researchers have principally considered illusions as useful tools for exploring the cognitive processing underlying vision. Our findings highlight the possibility that they have important ecological implications, affecting the everyday interactions of an animal with its physical world besides its intra- and interspecific relationships.

Color preference and manual laterality in the emperor tamarin (Saguinus imperator).

The current research focuses on color preference between red and green stimuli and manual laterality in the emperor tamarin (Saguinus imperator). Trichromacy in primates has been related to a foraging advantage allowing frugivore primates to distinguish ripe from unripe fruits as well to socio-sexual communication, as trichromats would be advantaged in recognizing social and sexual signals. As warm colors can affect the emotive state of the subjects, leading to the activation of one hemisphere over the other (e.g., right hemisphere), this could lead to behavioral lateralization. Thus, studying of hand preference may be relevant when testing color preference. Nine adult zoo emperor tamarins were involved and the study aimed to investigate the preference between red, green, and white cones as well as manual laterality. Tamarins were provided with pairs of red-green, red-white, and green-white combinations of cones. Ten 30-min sessions per combination were carried out and data on the interaction with one of the two cones of each apparatus were collected to assess subjects' color preference. We also recorded the hand used by each subject during the interaction with cones of different colors and the position of the apparatus in respect to the tamarin. We found no preferences for colored versus white cones. Similarly, we reported no group-level preferences within different color combinations, whereas individual-level preferences were found when considering all choices. Finally, we found that red cones elicited a left-hand preference, suggesting a right-hemisphere involvement in the presence of red cones. Although we do not have genetic data on trichromat and dichromat females, the tendency to use the left hand when interacting with red stimuli provides further evidence that warm colors can influence the emotive state of the perceiver, affecting their manual lateralization.

Are cerebral and behavioural lateralization related to anxiety-like traits in the animal model zebrafish (Danio rerio)?

Brain lateralization refers to hemispheric asymmetries in functions and/or neuroanatomical structures. Functional specialization in non-human animals has been mainly inferred through observation of lateralized motor responses and sensory perception. Only in a few cases has the influence of brain asymmetries on behaviour been described. Zebrafish has rapidly become a valuable model to investigate this issue as it displays epithalamic asymmetries that have been correlated to some lateralized behaviours. Here we investigated the relation between neuroanatomical or behavioural lateralization and anxiety using a light-dark preference test in adult zebrafish. In Experiment 1, we observed how scototaxis response varied as a function of behavioural lateralization measured in the detour task as turning preference in front of a dummy predator. In Experiment 2, foxD3:GFP transgenic adult zebrafish with left or right parapineal position, were tested in the same light-dark test as fish in Experiment 1. No correlation was found between the behaviour observed in the detour test and in the scototaxis test nor between the left- and right-parapineal fish and the scototaxis response. The consistency of results obtained in both experiments indicates that neither behavioural nor neuroanatomical asymmetries are related to anxiety-related behaviours measured in the light-dark test.

The ontogeny of continuous quantity discrimination in zebrafish larvae (Danio rerio).

Several studies have investigated the ontogeny of the capacity to discriminate between discrete numerical information in human and non-human animals. Contrarily, less attention has been devoted to the development of the capacity to discriminate continuous quantities. Recently, we set up a fast procedure for screening continuous quantity abilities in adult individuals of an animal model in neurodevelopmental research, the zebrafish. Two different sized holes are presented in a wall that divides the home tank in two halves and the spontaneous preference of fish for passing through the larger hole is exploited to measure their discrimination ability. We tested zebrafish larvae in the first, second and third week of life varying the relative size of the smaller circle (0.60, 0.75, 0.86, 0.91 area ratio). We found that the number of passages increased across the age. The capacity to discriminate the larger hole decreased as the ratio between the areas increased. No difference in accuracy was found as a function of age. The accuracy of larval zebrafish almost overlaps that found in adults in a previous study, suggesting a limited role of maturation and experience on the ability to estimate areas in this species.

Everything is subjective under water surface, too: visual illusions in fish.

The study of visual illusions has captured the attention of comparative psychologists since the last century, given the unquestionable advantage of investigating complex perceptual mechanisms with relatively simple visual patterns. To date, the observation of animal behavior in the presence of visual illusions has been largely confined to mammal and bird studies. Recently, there has been increasing interest in investigating fish, too. The attention has been particularly focused on guppies, redtail splitfin and bamboo sharks. Overall, the tested species were shown to experience a human-like perception of different illusory phenomena involving size, number, motion, brightness estimation and illusory contours. However, in some cases, no illusory effects, or evidence for a reverse illusion, were also reported. Here, we review the current state of the art in this field. We conclude that a wider investigation of visual illusions in fish is fundamental to form a broader comprehension of perceptual systems of vertebrates. Furthermore, we believe that this type of investigation could help us to address general important issues in perceptual studies, such as the role of ecology in shaping perceptual systems, the existence of interindividual variability in the visual perception of nonhuman species and the role of cortical activity in the emergence of visual illusions.

Correction to: Linear numerosity illusions in capuchin monkeys (Sapajus apella), rhesus macaques (Macaca mulatta), and humans (Homo sapiens).

In the original publication, values of last three rows in Table 1 and Table 2 were incorrectly published.

Linear numerosity illusions in capuchin monkeys (Sapajus apella), rhesus macaques (Macaca mulatta), and humans (Homo sapiens).

Numerosity illusions emerge when the stimuli in one set are overestimated or underestimated relative to the number (or quantity) of stimuli in another set. In the case of multi-item arrays, individual items that form a better Gestalt are more readily grouped, leading to overestimation by human adults and children. As an example, the Solitaire illusion emerges when dots forming a central cluster (cross-pattern) are overestimated relative to the same number of dots on the periphery of the array. Although this illusion is robustly experienced by human adults, previous studies have produced weaker illusory results for young children, chimpanzees, rhesus macaques, capuchin monkeys, and guppies. In the current study, we presented nonhuman primates with other linear arrangements of stimuli from Frith and Frith's (Percept Psychoph 11:409-410, 1972) original paper with human participants that included the Solitaire illusion. Capuchin monkeys, rhesus macaques, and human adults learned to quantify black and white dots that were presented within intermingled arrays, responding on the basis of the more numerous dot colors. Humans perceived the various illusions similar to the original findings of Frith and Frith (1972), validating the current comparative design; however, there was no evidence of illusory susceptibility in either species of monkey. These results are considered in light of illusion susceptibility among primates as well as considering the role of numerical discrimination abilities and perceptual processing mode on illusion emergence.

Guppies, Poecilia reticulata, perceive a reversed Delboeuf illusion.

Animals are often required to estimate object sizes during several fitness-related activities, such as choosing mates, foraging, and competing for resources. Some species are susceptible to size illusions, i.e. the misperception of the size of an object based on the surrounding context, but other species are not. This interspecific variation might be adaptive, reflecting species-specific selective pressures; according to this hypothesis, it is important to test species in which size discrimination has a notable ecological relevance. We tested susceptibility to a size illusion in the guppy, Poecilia reticulata, a fish species required to accurately estimate sizes during mate choice, foraging, and antipredator behaviours. We focussed on the Delboeuf illusion, in which an object is typically perceived to be larger when surrounded by a smaller object. In experiment 1, we trained guppies to select the larger of two circles to obtain a food reward and then tested them using stimuli arranged in a Delboeuf-like pattern. In experiment 2, we tested guppies in a spontaneous food choice task to determine whether the subjective size perception of food items is affected by the surrounding context. Jointly, our experiments indicated that guppies perceived the Delboeuf illusion, but in a reverse direction relative to humans: guppies estimated as larger the stimulus that human perceived as smaller. Our results indicated susceptibility to size illusions also in a species required to perform accurate size discrimination and support previous evidence of variability in illusion susceptibility across vertebrates.

Honeybees use absolute rather than relative numerosity in number discrimination.

Various vertebrate species use relative numerosity judgements in comparative assessments of quantities for which they use larger/smaller relationships rather than absolute number. The numerical ability of honeybees shares basic properties with that of vertebrates but their use of absolute or relative numerosity has not been explored. We trained free-flying bees to choose variable images containing three dots; one group ('larger') was trained to discriminate 3 from 2, while another group ('smaller') was trained to discriminate 3 from 4. In both cases, numbers were kept constant but stimulus characteristics and position were varied from trial to trial. Bees were then tested with novel stimuli displaying the previously trained numerosity (3) versus a novel numerosity (4 for 'larger' and 2 for 'smaller'). Both groups preferred the three-item stimulus, consistent with absolute numerosity. They also exhibited ratio-dependent discrimination of numbers, a property shared by vertebrates, as performance after 2 versus 3 was better than after 3 versus 4 training. Thus, bees differ from vertebrates in their use of absolute rather than of relative numerosity but they also have some numeric properties in common.

Exploring the Jastrow Illusion in Humans ( Homo sapiens), Rhesus Monkeys ( Macaca mulatta), and Capuchin Monkeys ( Sapajus apella).

In the Jastrow size illusion, two vertically stacked but offset stimuli of identical size are misperceived such that the bottom stimulus is overestimated relative to the top stimulus due to their spatial layout. In this study, we explored whether nonhuman primates perceive this geometric illusion in the same manner as humans. Human adults, rhesus macaques, and capuchin monkeys were presented with a computerized size discrimination task including Jastrow illusion probe trials. Consistent with previous results, humans perceived the illusory stimuli, validating the current experimental approach. Adults selected the bottom figure as larger in illusion trials with identical shapes, and performance was facilitated in trials with a true size difference when the larger figure was positioned at bottom. Monkeys performed very well in trials with a true size difference including difficult discriminations (5% difference in stimuli size), but they did not show evidence of the Jastrow illusion. They were indifferent between top and bottom stimuli in the illusory arrangement, showing no evidence of a human-like (or reversed) bias. These results are considered in light of differences in perceptual processing across primates and in comparison to previous comparative studies of the Jastrow and other size illusions.

Sex differences in discrimination reversal learning in the guppy.

In several mammalian and avian species, females show a higher performance than males in tasks requiring cognitive flexibility such as the discrimination reversal learning. A recent study showed that female guppies are twice as efficient as males in a reversal learning task involving yellow-red discrimination, suggesting a higher cognitive flexibility in female guppies. However, the possibility exists that the superior performance exhibited by females does not reflect a general sex difference in cognitive abilities, but instead, is confined to colour discrimination tasks. To address this issue, we compared male and female guppies in two different discrimination reversal learning tasks and we performed a meta-analysis of these experiments and the previous one involving colour discrimination. In the first experiment of this study, guppies were tested in a task requiring them to learn to select the correct arm of a T-maze in order to rejoin a group of conspecifics. In experiment 2, guppies were observed in a numerical task requiring them to discriminate between 5 and 10 dots in order to obtain a food reward. Although females outperformed males in one condition of the T-maze, we did not find any clear evidence of females' greater reversal learning performance in either experiment. However, the meta-analysis of the three experiments supported the hypothesis of females' greater reversal learning ability. Our data do not completely exclude the idea that female guppies have a generally higher cognitive flexibility than males; however, they suggest that the size of this sex difference might depend on the task.

Do domestic dogs (Canis lupus familiaris) perceive the Delboeuf illusion?

In the last decade, visual illusions have been repeatedly used as a tool to compare visual perception among species. Several studies have investigated whether non-human primates perceive visual illusions in a human-like fashion, but little attention has been paid to other mammals, and sensitivity to visual illusions has been never investigated in the dog. Here, we studied whether domestic dogs perceive the Delboeuf illusion. In human and non-human primates, this illusion creates a misperception of item size as a function of its surrounding context. To examine this effect in dogs, we adapted the spontaneous preference paradigm recently used with chimpanzees. Subjects were presented with two plates containing food. In control trials, two different amounts of food were presented in two identical plates. In this circumstance, dogs were expected to select the larger amount. In test trials, equal food portion sizes were presented in two plates differing in size: if dogs perceived the illusion as primates do, they were expected to select the amount of food presented in the smaller plate. Dogs significantly discriminated the two alternatives in control trials, whereas their performance did not differ from chance in test trials with the illusory pattern. The fact that dogs do not seem to be susceptible to the Delboeuf illusion suggests a potential discontinuity in the perceptual biases affecting size judgments between primates and dogs.

Quantitative abilities in a reptile (Podarcis sicula).

The ability to identify the largest amount of prey available is fundamental for optimizing foraging behaviour in several species. To date, this cognitive skill has been observed in all vertebrate groups except reptiles. In this study we investigated the spontaneous ability of ruin lizards to select the larger amount of food items. In Experiment 1, lizards proved able to select the larger food item when presented with two alternatives differing in size (0.25, 0.50, 0.67 and 0.75 ratio). In Experiment 2 lizards presented with two groups of food items (1 versus 4, 2 versus 4, 2 versus 3 and 3 versus 4 items) were unable to select the larger group in any contrast. The lack of discrimination in the presence of multiple items represents an exception in numerical cognition studies, raising the question as to whether reptiles' quantitative abilities are different from those of other vertebrate groups.

The contribution of fish studies to the "number sense" debate.

Leibovich et al. propose that number sense is not innate but gradually emergent during ontogeny following experience. We argue that this hypothesis cannot be reasonably tested in humans, in which the contribution of neural maturation and experience cannot be experimentally manipulated. Studies on animals, especially fish, can more effectively provide critical insights into the innate nature of numerical abilities.

The elusive illusion: Do children (Homo sapiens) and capuchin monkeys (Cebus apella) see the Solitaire illusion?

One approach to gaining a better understanding of how we perceive the world is to assess the errors that human and nonhuman animals make in perceptual processing. Developmental and comparative perspectives can contribute to identifying the mechanisms that underlie systematic perceptual errors often referred to as perceptual illusions. In the visual domain, some illusions appear to remain constant across the lifespan, whereas others change with age. From a comparative perspective, many of the illusions observed in humans appear to be shared with nonhuman primates. Numerosity illusions are a subset of visual illusions and occur when the spatial arrangement of stimuli within a set influences the perception of quantity. Previous research has found one such illusion that readily occurs in human adults, the Solitaire illusion. This illusion appears to be less robust in two monkey species, rhesus macaques and capuchin monkeys. We attempted to clarify the ontogeny of this illusion from a developmental and comparative perspective by testing human children and task-naïve capuchin monkeys in a computerized quantity judgment task. The overall performance of the monkeys suggested that they perceived the numerosity illusion, although there were large differences among individuals. Younger children performed similarly to the monkeys, whereas older children more consistently perceived the illusion. These findings suggest that human-unique perceptual experiences with the world might play an important role in the emergence of the Solitaire illusion in human adults, although other factors also may contribute.

Relative versus absolute numerical representation in fish: Can guppies represent "fourness"?

In recent years, the use of operant conditioning procedures has shown that species as diverse as chimpanzees, honeybees, and mosquitofish can be trained to discriminate between sets containing different numbers of objects. However, to succeed in this task, subjects can use two different strategies: either select the array containing a specific number of items (an absolute numerosity rule), or select the set containing the larger (or smaller) quantity of items (a relative numerosity rule). In the latter case, subjects need not only be able to judge whether two numerosities are equal or different but also be able to order numerosities. Here, in two experiments, we address whether fish can perform both kinds of judgment by training them with specific numerosities and testing their generalization to new numerosity contrasts. In Experiment 1, subjects were initially trained to select between visual arrays of 6 and 12 shapes, and were then tested with a contrast pairing the previously trained numerosity (either 6 or 12) with a novel numerosity (respectively, 3 or 24). Spontaneously, subjects selected the novel numerosity, in accordance with a relative numerosity rule. The second experiment tested whether guppies can also learn to select one specific number against all others, if appropriately trained. Fish trained to select an array of 4 shapes against several alternatives (4 vs. 1, 4 vs. 2, 4 vs. 8, 4 vs. 10) learned to recognize the number 4 against all alternatives and proved able to generalize their discrimination to novel, more difficult contrasts (4 vs. 3 and 4 vs. 6 items). In summary, although guppies preferentially opt for relative comparisons, they can flexibly learn either relative or absolute decision criteria on numerosity stimuli, depending on the context.

Do rhesus monkeys (Macaca mulatta) perceive illusory motion?

During the last decade, visual illusions have been used repeatedly to understand similarities and differences in visual perception of human and non-human animals. However, nearly all studies have focused only on illusions not related to motion perception, and to date, it is unknown whether non-human primates perceive any kind of motion illusion. In the present study, we investigated whether rhesus monkeys (Macaca mulatta) perceived one of the most popular motion illusions in humans, the Rotating Snake illusion (RSI). To this purpose, we set up four experiments. In Experiment 1, subjects initially were trained to discriminate static versus dynamic arrays. Once reaching the learning criterion, they underwent probe trials in which we presented the RSI and a control stimulus identical in overall configuration with the exception that the order of the luminance sequence was changed in a way that no apparent motion is perceived by humans. The overall performance of monkeys indicated that they spontaneously classified RSI as a dynamic array. Subsequently, we tested adult humans in the same task with the aim of directly comparing the performance of human and non-human primates (Experiment 2). In Experiment 3, we found that monkeys can be successfully trained to discriminate between the RSI and a control stimulus. Experiment 4 showed that a simple change in luminance sequence in the two arrays could not explain the performance reported in Experiment 3. These results suggest that some rhesus monkeys display a human-like perception of this motion illusion, raising the possibility that the neurocognitive systems underlying motion perception may be similar between human and non-human primates.