Function and flexibility of object exploration in kea and New Caledonian crows.

A range of non-human animals frequently manipulate and explore objects in their environment, which may enable them to learn about physical properties and potentially form more abstract concepts of properties such as weight and rigidity. Whether animals can apply the information learned during their exploration to solve novel problems, however, and whether they actually change their exploratory behaviour to seek functional information about objects have not been fully explored. We allowed kea (Nestor notabilis) and New Caledonian crows (Corvus moneduloides) to explore sets of novel objects both before and after encountering a task in which some of the objects could function as tools. Following this, subjects were given test trials in which they could choose among the objects they had explored to solve a tool-use task. Several individuals from both species performed above chance on these test trials, and only did so after exploring the objects, compared with a control experiment with no prior exploration phase. These results suggest that selection of functional tools may be guided by information acquired during exploration. Neither kea nor crows changed the duration or quality of their exploration after learning that the objects had a functional relevance, suggesting that birds do not adjust their behaviour to explicitly seek this information.

Reasoning by exclusion in the kea (Nestor notabilis).

Reasoning by exclusion, i.e. the ability to understand that if there are only two possibilities and if it is not A, it must be B, has been a topic of great interest in recent comparative cognition research. Many studies have investigated this ability, employing different methods, but rarely exploring concurrent decision processes underlying choice behaviour of non-human animals encountering inconsistent or incomplete information. Here, we employed a novel training and test method in order to perform an in-depth analysis of the underlying processes. Importantly, to discourage the explorative behaviour of the kea, a highly neophilic species, the training included a large amount of novel, unrewarded stimuli. The subsequent test consisted of 30 sessions with different sequences of four test trials. In these test trials, we confronted the kea with novel stimuli that were paired with either the rewarded or unrewarded training stimuli or with the novel stimuli of previous test trials. Once habituated to novelty, eight out of fourteen kea tested responded to novel stimuli by inferring their contingency via logical exclusion of the alternative. One individual inferred predominantly in this way, while other response strategies, such as one trial learning, stimulus preferences and avoiding the negative stimulus also guided the responses of the remaining individuals. Interestingly, the difficulty of the task had no influence on the test performance. We discuss the implications of these findings for the current hypotheses about the emergence of inferential reasoning in some avian species, considering causal links to brain size, feeding ecology and social complexity.

Chronic West Nile virus infection in kea (Nestor notabilis).

Six kea (Nestor notabilis) in human care, naturally infected with West Nile virus (WNV) lineage 2 in Vienna, Austria, in 2008, developed mild to fatal neurological signs. WNV RNA persisted and the virus evolved in the birds' brains, as demonstrated by (phylo)genetic analyses of the complete viral genomes detected in kea euthanized between 2009 and 2014. WNV antibodies persisted in the birds, too. Chronic WNV infection in the brain might contribute to the circulation of the virus through oral transmission to predatory birds.

A new approach to comparing problem solving, flexibility and innovation.

Comparative cognition aims at unfolding the cognitive processes underlying animal behavior and their evolution, and is concerned with testing hypotheses about the evolution of the brain and intelligence in general. It is a developing field still challenged by conceptual and methodological issues. Systematic cross-species comparisons of cognitive abilities, taking both phylogeny and ecology into account are still scarce. One major reason for this is that it is very hard to find universally applicable paradigms that can be used to investigate the same cognitive ability or 'general intelligence' in several species. Many comparative paradigms have not paid sufficient attention to interspecific differences in anatomical, behavioral and perceptual features, besides psychological variables such as motivation, attentiveness or neophobia, thus potentially producing misrepresentative results. A new stance for future comparative research may be to establish behavioral and psychological profiles prior or alongside to comparing specific cognitive skills across species. Potentially revealing profiles could be obtained from examining species differences in how novel experimental (extractive foraging) tasks are explored and approached, how solutions are discovered and which ones are preferred, how flexibly multiple solutions are used and how much individual variation occurs, before proceeding to more detailed tests. Such new comparative approach is the Multi-Access-Box. It presents the animal with a novel problem that can be solved in several ways thus offering the possibility to examine species differences in all the above, and extract behavioral and perceptual determinants of their performance. Simultaneously, it is a suitable paradigm to collect comparative data about flexibility, innovativeness and problem solving ability, i.e., theoretical covariates of 'general intelligence', in a standardized manner.

Flexibility in problem solving and tool use of kea and New Caledonian crows in a multi access box paradigm.

Parrots and corvids show outstanding innovative and flexible behaviour. In particular, kea and New Caledonian crows are often singled out as being exceptionally sophisticated in physical cognition, so that comparing them in this respect is particularly interesting. However, comparing cognitive mechanisms among species requires consideration of non-cognitive behavioural propensities and morphological characteristics evolved from different ancestry and adapted to fit different ecological niches. We used a novel experimental approach based on a Multi-Access-Box (MAB). Food could be extracted by four different techniques, two of them involving tools. Initially all four options were available to the subjects. Once they reached criterion for mastering one option, this task was blocked, until the subjects became proficient in another solution. The exploratory behaviour differed considerably. Only one (of six) kea and one (of five) NCC mastered all four options, including a first report of innovative stick tool use in kea. The crows were more efficient in using the stick tool, the kea the ball tool. The kea were haptically more explorative than the NCC, discovered two or three solutions within the first ten trials (against a mean of 0.75 discoveries by the crows) and switched more quickly to new solutions when the previous one was blocked. Differences in exploration technique, neophobia and object manipulation are likely to explain differential performance across the set of tasks. Our study further underlines the need to use a diversity of tasks when comparing cognitive traits between members of different species. Extension of a similar method to other taxa could help developing a comparative cognition research program.

Navigating a tool end in a specific direction: stick-tool use in kea (Nestor notabilis).

This study depicts how captive kea, New Zealand parrots, which are not known to use tools in the wild, employ a stick-tool to retrieve a food reward after receiving demonstration trials. Four out of six animals succeeded in doing so despite physical (beak curvature) and ecological (no stick-like materials used during nest construction) constraints when handling elongated objects. We further demonstrate that the same animals can thereafter direct the functional end of a stick-tool into a desired direction, aiming at a positive option while avoiding a negative one.

Big brains are not enough: performance of three parrot species in the trap-tube paradigm.

The trap-tube task has become a benchmark test for investigating physical causality in vertebrates. In this task, subjects have to retrieve food out of a horizontal tube using a tool and avoiding a trap hole in the tube. Great apes and corvids succeeded in this task. Parrots with relative brain volumes comparable to those of corvids and primates also demonstrate high cognitive abilities. We therefore tested macaws, a cockatoo, and keas on the trap-tube paradigm. All nine parrots failed to solve the task. In a simplified task, trap tubes with a slot inserted along the top were offered. The slot allowed the birds to move the reward directly with their bills. All but one individual solved this task by lifting the food over the trap. However, the parrots failed again when they were prevented from lifting the reward, although they anticipated that food will be lost when moved into the trap. We do not think that the demanding use of an external object is the main reason for the parrots' failure. Moreover, we suppose these parrots fail to consider the trap's position in the beginning of a trial and were not able to stop their behaviour and move the reward in the trap's opposite direction.

How do keas (Nestor notabilis) solve artificial-fruit problems with multiple locks?

Keas, a species of parrots from New Zealand, are an interesting species for comparative studies of problem solving and cognition because they are known not only for efficient capacities for object manipulation but also for explorative and playful behaviors. To what extent are they efficient or explorative, and what cognitive abilities do they use? We examined how keas would solve several versions of artificial-fruit box problems having multiple locks. After training keas to remove a metal rod from over a Plexiglas lid that had to be opened, we exposed the birds to a variety of tasks having two or more locks. We also introduced a preview phase during which the keas had extended opportunity to look at the tasks before the experimenter allowed the birds to solve them, to examine whether the preview phase would facilitate the birds' performance on the tasks. In a large number of tests, the keas showed a strong trend to solve the tasks with no positive effect of previewing the tasks. When the tasks became complex, however, the keas corrected inappropriate responses more quickly when they had had chance to preview the problems than when they had not. The results suggest that the keas primarily used explorative strategies in solving the lock problems but might have obtained some information about the tasks before starting to solve them. This may reflect a good compromise of keas' trial-and-error tendency and their good cognitive ability that result from a selection pressure they have faced in their natural habitat.

What you see is what you get? Exclusion performances in ravens and keas.

BACKGROUND: Among birds, corvids and parrots are prime candidates for advanced cognitive abilities. Still, hardly anything is known about cognitive similarities and dissimilarities between them. Recently, exclusion has gained increasing interest in comparative cognition. To select the correct option in an exclusion task, one option has to be rejected (or excluded) and the correct option may be inferred, which raises the possibility that causal understanding is involved. However, little is yet known about its evolutionary history, as only few species, and mainly mammals, have been studied. METHODOLOGY/PRINCIPAL FINDINGS: We tested ravens and keas in a choice task requiring the search for food in two differently shaped tubes. We provided the birds with partial information about the content of one of the two tubes and asked whether they could use this information to infer the location of the hidden food and adjust their searching behaviour accordingly. Additionally, this setup allowed us to investigate whether the birds would appreciate the impact of the shape of the tubes on the visibility of food. The keas chose the baited tube more often than the ravens. However, the ravens applied the more efficient strategy, choosing by exclusion more frequently than the keas. An additional experiment confirmed this, indicating that ravens and keas either differ in their cognitive skills or that they apply them differently. CONCLUSION: To our knowledge, this is the first study to demonstrate that corvids and parrots may perform differently in cognitive tasks, highlighting the potential impact of different selection pressures on the cognitive evolution of these large-brained birds.

Kea (Nestor notabilis) consider spatial relationships between objects in the support problem.

The 'Support Problem' is a benchmark test to investigate the understanding of spatial relationships between objects. We tested kea parrots' performance in a paradigm that has previously been studied in primates. Kea perform comparably well to tamarins when they are confronted with a choice between two support devices, one of which has a reward resting on it and the other slightly next to it, or when given a choice between a continuous and a disrupted support. Kea did better than chimpanzees in some tasks in which the perceptual connection of the food to the support was altered. The results indicate that kea are capable of assessing the spatial means-end relationships of this problem spontaneously and in a way that is comparable with primates.

Social attention in keas, dogs, and human children.

Understanding animals' abilities to cooperate with and learn from each other has been an active field of research in recent years. One important basis for all types of social interactions is the disposition of animals to pay attention to each other-a factor often neglected in discussions and experiments. Since attention differs between species as well as between individuals, it is likely to influence the amount and type of information different species and/or observers may extract from conspecifics in any given situation. Here, we carried out a standardized comparative study on attention towards a model demonstrating food-related behavior in keas, dogs and children. In a series of experimental sessions, individuals watched different conspecific models while searching, manipulating and feeding. Visual access to the demonstration was provided by two observation holes, which allowed us to determine exactly how often and for how long observers watched the model. We found profound differences in the factors that influence attention within as well as between the tested species. This study suggests that attention should be incorporated as an important variable when testing species in social situations.

Technical intelligence in animals: the kea model.

The ability to act on information flexibly is one of the cornerstones of intelligent behavior. As particularly informative example, tool-oriented behavior has been investigated to determine to which extent nonhuman animals understand means-end relations, object affordances, and have specific motor skills. Even planning with foresight, goal-directed problem solving and immediate causal inference have been a focus of research. However, these cognitive abilities may not be restricted to tool-using animals but may be found also in animals that show high levels of curiosity, object exploration and manipulation, and extractive foraging behavior. The kea, a New Zealand parrot, is a particularly good example. We here review findings from laboratory experiments and field observations of keas revealing surprising cognitive capacities in the physical domain. In an experiment with captive keas, the success rate of individuals that were allowed to observe a trained conspecific was significantly higher than that of naive control subjects due to their acquisition of some functional understanding of the task through observation. In a further experiment using the string-pulling task, a well-probed test for means-end comprehension, we found the keas finding an immediate solution that could not be improved upon in nine further trials. We interpreted their performance as insightful in the sense of being sensitive of the relevant functional properties of the task and thereby producing a new adaptive response without trial-and-error learning. Together, these findings contribute to the ongoing debate on the distribution of higher cognitive skills in the animal kingdom by showing high levels of sensorimotor intelligence in animals that do not use tools. In conclusion, we suggest that the 'Technical intelligence hypothesis' (Byrne, Machiavellian intelligence II: extensions and evaluations, pp 289-211, 1997), which has been proposed to explain the origin of the ape/monkey grade-shift in intelligence by a selection pressure upon an increased efficiency in foraging behavior, should be extended, that is, applied to some birds as well.

Limited spread of innovation in a wild parrot, the kea (Nestor notabilis).

In the local population of kea in Mount Cook Village, New Zealand, some keas open the lids of rubbish bins with their bill to obtain food scraps within. We investigated the extent to which this innovation has spread in the local population, and what factors limit the acquisition of bin opening. Only five males of 36 individually recognised birds were observed to have performed successful bin opening. With one exception there were always other keas present, watching successful bin opening. Seventeen additional individuals were seen to have benefitted from lid opening. Their foraging success was less than that of the bin openers. Social status of bin openers did not differ from scrounging males. Among the individuals that were regularly seen at the site of the bins but were not successful in bin opening, social status and the ratio of feeding directly from open bins correlated with the amount of opening attempts. We conclude that scrounging facilitated certain behavioural aspects of bin opening rather than inhibiting them. The fact that only 9% of opening attempts were successful, and the long period of time required to increase efficiency in lid opening shows that mainly individual experience, and to a lesser extent insight and social learning, play key roles in acquisition of the opening technique. The results indicate that the spread of innovative solutions of challenging mechanical problems in animals may be restricted to only a few individuals.

Testing social learning in a wild mountain parrot, the kea (Nestor notabilis).

Huber, Taborsky, and Rechberger (2001) reported an experiment in which the efficiency with which captive keas opened a complex food container was increased by observation of a skilled conspecific. However, only testing social learning in free-ranging animals can demonstrate social learning in natural conditions. For that purpose, a tube-lifting paradigm was developed and tested on keas both in captivity and in Mount Cook National Park, New Zealand. The task was to remove a tube from an upright pole in order to gain access to a reward inside the tube. The top of the pole was higher than a standing kea, so that, to remove the tube, an individual had to simultaneously climb onto the pole and manipulate the tube up the pole with its bill. Because only 1 naive bird managed to remove a tube twice in 25 half-hour sessions and disappeared after success, another bird was trained to solve the task and to provide demonstrations for others. Even under such conditions, only 2 of at least 15 birds learned to remove the tube in 28 sessions. There was no indication that observer birds' use of bill and feet when exploring the tube changed as the number of observations of tube removal increased in a way that would, in principle, increase the likelihood of tube removal. The results suggest a dissociation of social learning potential as assessed in laboratory animals, and social transmission of foraging techniques in natural populations.