Understanding of and reasoning about object-object relationships in long-tailed macaques?

Diagnostic reasoning, defined as the ability to infer unobserved causes based on the observation of their effects, is a central cognitive competency of humans. Yet, little is known about diagnostic reasoning in non-human primates, and what we know is largely restricted to the Great Apes. To track the evolutionary history of these skills within primates, we investigated long-tailed macaques' understanding of the significance of inclinations of covers of hidden food as diagnostic indicators for the presence of an object located underneath. Subjects were confronted with choices between different objects that might cover food items. Based on their physical characteristics, the shape and orientation of the covers did or did not reveal the location of a hidden reward. For instance, hiding the reward under a solid board led to its inclination, whereas a hollow cup remained unaltered. Thus, the type of cover and the occurrence or absence of a change in their appearance could potentially be used to reason diagnostically about the location of the reward. In several experiments, the macaques were confronted with a varying number of covers and their performance was dependent on the level of complexity and on the type of change of the covers' orientation. The macaques could use a board's inclination to detect the reward, but failed to do so if the lack of inclination was indicative of an alternative hiding place. We suggest that the monkeys' performance is based on a rudimentary understanding of causality, but find no good evidence for sophisticated diagnostic reasoning in this particular domain.

Grey parrots use inferential reasoning based on acoustic cues alone.

Our ability to make logical inferences is considered as one of the cornerstones of human intelligence, fuelling investigations of reasoning abilities in non-human animals. Yet, the evidence to date is equivocal, with apes as the prime candidates to possess these skills. For instance, in a two-choice task, apes can identify the location of hidden food if it is indicated by a rattling noise caused by the shaking of a baited container. More importantly, they also use the absence of noise during the shaking of the empty container to infer that this container is not baited. However, since the inaugural report of apes solving this task, to the best of our knowledge, no comparable evidence could be found in any other tested species such as monkeys and dogs. Here, we report the first successful and instantaneous solution of the shaking task through logical inference by a non-ape species, the African grey parrot. Surprisingly, the performance of the birds was sensitive to the shaking movement: they were successful with containers shaken horizontally, but not with vertical shaking resembling parrot head-bobbing. Thus, grey parrots seem to possess ape-like cross-modal reasoning skills, but their reliance on these abilities is influenced by low-level interferences.

Is caching the key to exclusion in corvids? The case of carrion crows (Corvus corone corone).

Recently, two corvid species, food-caching ravens and non-caching jackdaws, have been tested in an exclusion performance (EP) task. While the ravens chose by exclusion, the jackdaws did not. Thus, foraging behaviour may affect EP abilities. To investigate this possibility, another food-caching corvid species, the carrion crow (Corvus corone corone), was tested in the same exclusion task. We hid food under one of two cups and subsequently lifted either both cups, or the baited or the un-baited cup. The crows were significantly above chance when both cups were lifted or when only the baited cup was lifted. When the empty cup was lifted, we found considerable inter-individual variation, with some birds having a significant preference for the un-baited but manipulated cup. In a follow-up task, we always provided the birds with the full information about the food location, but manipulated in which order they saw the hiding or the removal of food. Interestingly, they strongly preferred the cup which was manipulated last, even if it did not contain any food. Therefore, we repeated the first experiment but controlled for the movement of the cups. In this case, more crows found the food reliably in the un-baited condition. We conclude that carrion crows are able to choose by exclusion, but local enhancement has a strong influence on their performance and may overshadow potential inferential abilities. However, these findings support the hypothesis that caching might be a key to exclusion in corvids.

Early development of gaze following into distant space in juvenile Greylag geese (Anser anser).

Visual co-orientation with another's gaze direction (gaze following) may provide important information about the location of food, social interactions or predators. Gaze following has been shown in a variety of mammals, but only in few bird species, and has not been tested in precocial birds at all. It has been suggested that gaze following is an anti-predator behaviour, and in Common ravens (Corvus corax) and rooks (C. frugilegus), it emerges shortly after fledging, at a time when young birds leave the predator-safe nest. However, if gaze following is adaptive, the developmental pattern should differ between altricial and precocial birds. Greylag geese (Anser anser) are highly social birds with a precocial development. Goslings move and feed independently within 24 h post-hatching, and they are highly vulnerable to aerial predators. We therefore predicted that greylag geese are capable of gaze following and that they develop this skill already pre-fledging. We experimentally tested 19 hand-raised greylag goslings for their ability to follow a conspecific's gaze when they were between 10 days and 6 weeks old. In line with our predictions, first responses were already detectable in 10-day-old goslings. Our results therefore not only demonstrate that greylag geese follow the gaze of conspecifics into distant space, but that they also develop this ability much earlier than altricial birds.

African grey parrots (Psittacus erithacus) use inference by exclusion to find hidden food.

Exclusion allows the detection of hidden food when confronted with the choice between an empty and a potentially baited food location. However, exclusion may be based on avoidance of the empty location without drawing inferences about the presence of the food in the baited location. So far, such inferences have been demonstrated in the great apes only: after seeing an experimenter eating one of two food types, which both had been hidden previously in two boxes, the apes were able to choose the box that still contained the other food type. African grey parrots are capable of exclusion, and we here assessed if they are capable of inference by exclusion. In our task, two different but equally preferred food items were hidden in full view of the birds under two opaque cups. Then, an experimenter secretly removed one food type and showed it to the bird. Similarly to the apes, one out of seven parrots significantly preferred the baited cup; control conditions rule out that its choice was based on associative learning or the use of olfactory cues. Thus, we conclude that-like the apes-some grey parrots are able to infer the location of a hidden food reward.

Ravens judge competitors through experience with play caching.

Complex social behavior builds on the mutual judgment of individuals as cooperation partners and competitors [1]. Play can be used for assessing the others' dispositions in humans and nonhuman mammals [2], whereas little is known about birds. Recently, food-caching corvids have been found to rival primates in their ability to judge the behaviors and intentions of others in competition for hidden food [3]. Here, we show that ravens Corvus corax quickly learn to assess the competitive strategies of unfamiliar individuals through interactions with them over caches with inedible items and subsequently apply this knowledge when caching food. We confronted birds with two human experimenters who acted differently when birds cached plastic items: the pilferer stole the cached objects, whereas the onlooker did not. Birds responded to the actions of both experimenters with changing the location of their next object caches, either away from or toward the humans, as if they were testing their pilfering dispositions. In contrast, ravens instantly modified their caching behavior with food, preventing only the competitive human from finding the caches. Playful object caching in a social setting could thus aid ravens in evaluating others' pilfering skills.

Northern bald ibises follow others' gaze into distant space but not behind barriers.

Gaze following is the ability to use the visual orientation of others as a trigger to look in the same direction. Thereby, animals may either align their head and eye orientation with others (gaze following into distant space) or may even reposition themselves to look behind barriers impairing their perception (geometrical gaze following). It has been proposed that these two different modes are functionally and cognitively distinct, but experimental evidence for this claim is lacking. We here, to our knowledge, demonstrate for the first time, that adult animals may be capable of following gaze into distant space, but not geometrically around barriers. We tested Northern bald ibises (Geronticus eremita) for their ability to follow a conspecific's gaze in two standard tasks. The birds readily looked up after seeing a model bird looking up; however, when seeing a model looking behind a barrier, they responded by looking at the barrier instead of walking around. These findings are in stark contrast to results obtained with great apes and corvids and provide the first experimental evidence, to our knowledge, for cognitive differences in gaze following tasks.

Modifying the object-choice task: is the way you look important for ravens?

Most animals seem to have difficulties in using gaze cues to find hidden food in object-choice tasks. For instance, chimpanzees usually fail in these tests, even though they are capable of following other's gaze geometrically behind barriers. Similar to chimpanzees, common ravens are skilled in tracking other's gaze but fail in object-choice tasks. We here explored whether procedural modifications, which had been used successfully in chimpanzees, would also yield positive results in ravens. In our modifications (a) the experimenter approached the cup while gazing at it, (b) the gaze cue was accompanied by a sound and (c) the experimenter could actually see the food while giving the gaze cue. Two out of seven birds performed above chance level in some of these conditions. However, we ascribe this improvement to the individuals' learning ability rather than to an understanding of the communicative nature of the task. This interpretation is further supported by results of a follow-up experiment suggesting that ravens may not rely on conspecifics' gaze cues for finding food caches in a natural foraging context. In sum, our results suggest that ravens may not transfer their gaze follow abilities to foraging situations involving hidden food.

Novel object exploration in ravens (Corvus corax): effects of social relationships.

Social context has been shown to encourage, or to delay object exploration and learning. This ambiguity might be due to factors such as social relationships and personality of the individuals involved. Here, we investigated in ravens (Corvus corax) individuals' consistency in response to novel objects over development and across contexts: alone versus social. In the social setting we focussed on the effects of social relationships on social facilitation during the approach to novel objects. We tested 11 hand-raised ravens with novel objects individually at three and six months of age and in dyadic combinations at six months of age. Individuals were consistent over development and contexts in their response to different novel objects. Birds joined siblings faster to approach novel objects than non-siblings. They also spent more time sitting close to siblings than to non-siblings. In male-male dyads but not in female-female dyads, subordinates approached the novel objects significantly faster than dominant birds. In contrast, dominant males were the first to approach the novel objects in mixed-sex combinations. Hence, the effect of social context seems to depend on the social relationships towards the companions and on the combination of the sexes.

Seeing the experimenter influences the response to pointing cues in long-tailed macaques.

Methodological variations in experimental conditions can strongly influence animals' performances in cognitive tests. Specifically, the procedure of the so-called object-choice task has been controversially discussed; here, a human experimenter indicates the location of hidden food by pointing or gazing at one of two or more containers. Whereas dogs usually succeed, results for nonhuman primates are ambiguous. In the standard version of the task the majority of subjects do not respond appropriately to human pointing. However, modifying the task setup, such as placing the containers further apart, seems to improve subjects' performances, suggesting that cue salience may be an important variable. Here we investigated whether the visibility of the experimenter inhibits long-tailed macaques' (Macaca fascicularis) usage of the pointing cue. In our baseline condition, with the experimenter fully visible, the monkeys chose the correct container in 61% of the trials. The performance increased significantly, however, when the experimenter was hidden behind a curtain and only the arm of the experimenter, a doll's arm, or a stick was visible. Furthermore, the monkeys performed significantly better when the tip of the pointing finger or device was close to the target compared to the more distant condition. Intriguingly, after these experiments the monkeys' performance was also significantly improved in the baseline condition (70%). Apparently, the monkeys were first distracted by the presence of the experimenter, but then learned to use the cue. These findings highlight the importance of the test conditions, and question some of the assumptions about species-specific differences in the object-choice task.

Transitive inference in jackdaws (Corvus monedula).

Transitive inference (TI) refers to the cognitive ability to derive relationships between items that have never been presented together before. TI could be a useful tool for individuals living in large social groups, as these are confronted with an increasing number of possible dyadic relationships between group members. Through TI, one could potentially identify rank relationships between group members and thereby avoid costly direct agonistic interactions. Jackdaws seem ideal candidates to test for the ability of TI as they live in relatively complex groups, in which such skills could be useful. We presently report the results of jackdaws in a touch screen experiment. Three individuals were trained to memorise an ordered sequence of five differently coloured squares (A-E), which were presented in four pairs consisting of two adjacent colours each (A/B, B/C, C/D, D/E). After reaching the pre-defined criteria in each single colour pair in a time comparable to other species, they were confronted with an unknown pair of two non-adjacent colours (B/D). The birds were able to identify the relationship according to the previously learned sequence by preferring B over D.

Does the stimulus type influence horses' performance in a quantity discrimination task?

The ability to understand the relation between quantities has been documented in a wide range of species. Such quantity discrimination competences are commonly demonstrated by a choice of the larger quantity or numerosity in a two-choice task. However, despite their overall success, many subjects commit a surprisingly large number of errors even in simple discriminations such as 1 vs. 3. Recently, it had been suggested that this is a result of the testing procedure. When monkeys could choose between different quantities of edible rewards, they showed low-level success. If, however, they chose between inedible items and were rewarded with edible items, their performance increased. The same held true if they chose between edible items but were rewarded with other edible items (Schmitt and Fischer, 2011). This led to the suggestion that the monkeys may not have been able to mentally separate between choice- and reward-stimuli in the initial test situation. To investigate if this response pattern can also be found in non-primate species, we replicated the experiment with 12 Icelandic horses kept at a private horse-riding school. Horses are known to discriminate between quantities up to three, but are very distantly related to primates. Unexpectedly, we found only weak evidence for quantity discrimination skills and no effect of the type of stimuli. Only some subjects reliably selected the larger quantity in some, but not all quantity pairs. These findings are not only in contrast to the previously conducted study on monkeys, but also to other studies on horses. From this, we conclude that quantity discrimination competence may only be of minor importance for horses and highlight the influence of experimental conditions on the outcome of cognitive tests.

The influence of local enhancement on choice performances in African Grey parrots (Psittacus erithacus) and jackdaws (Corvus monedula).

Being attentive to the behavior of others may be advantageous to gain important information, for example, on the location of food. Often, this is achieved through simple local enhancement. However, this is not always beneficial, as it may override cognitive abilities, with negative consequences. Grey parrots (Psittacus erithacus) and ravens have already succeeded in exclusion tasks, but carrion crows do so only when controlling for local enhancement, and jackdaws (Corvus monedula) fail entirely. Presently, we tested whether jackdaws would still be influenced by local enhancement in a simple choice-task. We compared their performance with those of Grey parrots. Since these birds did not respond to enhancement in the exclusion task, we expected them also to be less susceptible to enhancement here. In our tasks, two pieces of food were visibly hidden under two cups. Then one cup was lifted, the reward was shown to the bird and was either laid back underneath the cup or was removed. Alternatively, both manipulations were combined with the first reward being shown to the bird and the second one being removed or vice versa. Surprisingly, both species had a preference for the last handled cup, irrespective of whether it contained food or not. However, if the birds had to wait for 10 seconds after the presentation, the jackdaws performed better than the Grey parrots. Additionally, the delay improved the performance of both species in conditions in which the reward was removed last and deteriorated their performance in conditions in which the item was shown last.

What you see is what you get--reloaded: can jackdaws (Corvus monedula) find hidden food through exclusion?

Choice by exclusion, that is, the ability to base the choice of a target on the rejection of potential alternatives, is becoming increasingly interesting for comparative cognition research. Recently, ravens have been shown to solve an exclusion task and it had been suggested that this ability might benefit ravens in a food-caching context. To investigate this possibility, the raven study was replicated with a closely related, but noncaching, species, the jackdaw (Corvus monedula). In the first test, the birds had to find food hidden in one of two differently shaped tubes. The results suggest that the jackdaws found the food through intensive search behavior, with little evidence for exclusion abilities. In a follow-up experiment, the tubes were replaced by cups, and before the birds made a choice, one of the cups was lifted to inform them about its content. In a final task, this procedure was modified to control for the influence of local enhancement. In both experiments, the jackdaws were successful only if they had seen the food before. These findings are in contrast to the previous results on ravens and support the idea that exclusion abilities may have evolved as specific adaptations to food caching.

Gaze direction - a cue for hidden food in rooks (Corvus frugilegus)?

Other individual's head- and eye-directions can be used as social cues indicating the presence of important events. Among birds, ravens and rooks have been shown to co-orient with conspecifics and with humans by following their gaze direction into distant space and behind visual screens. Both species use screens to cache food in private; also, it had been suggested that they may rely on gaze cues to detect hidden food. However, in an object-choice task, ravens failed to do so, and their competitive lifestyle may have prevented them from relying on these cues. Here we tested closely related and cooperative rooks. Food was hidden in one of two cups and the experimenter gazed at the baited cup. In a second experiment, we aimed to increase the birds' motivation to choose correctly by increasing the investment needed to obtain the reward. To do so, the birds had to pull on a string to obtain the cup. Here, the birds as a group tended to rely on gaze cues. In addition, individual birds quickly learned to use the cue in both experiments. Although rooks may not use gaze cues to find hidden food spontaneously, they may quickly learn to do so.

On the evolutionary and ontogenetic origins of tool-oriented behaviour in New Caledonian crows (Corvus moneduloides).

New Caledonian crows (Corvus moneduloides) are prolific tool users in captivity and in the wild, and have an inherited predisposition to express tool-oriented behaviours. To further understand the evolution and development of tool use, we compared the development of object manipulation in New Caledonian crows and common ravens (Corvus corax), which do not routinely use tools. We found striking qualitative similarities in the ontogeny of tool-oriented behaviour in New Caledonian crows and food-caching behaviour in ravens. Given that the common ancestor of New Caledonian crows and ravens was almost certainly a caching species, we therefore propose that the basic action patterns for tool use in New Caledonian crows may have their evolutionary origins in caching behaviour. Noncombinatorial object manipulations had similar frequencies in the two species. However, frequencies of object combinations that are precursors to functional behaviour increased in New Caledonian crows and decreased in ravens throughout the study period, ending 6 weeks post-fledging. These quantitative observations are consistent with the hypothesis that New Caledonian crows develop tool-oriented behaviour because of an increased motivation to perform object combinations that facilitate the necessary learning.

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.

Do common ravens (Corvus corax) rely on human or conspecific gaze cues to detect hidden food?

The ability of non-human animals to use experimenter-given cues in object-choice tasks has recently gained interest. In such experiments, the location of hidden food is indicated by an experimenter, e.g. by gazing, pointing or touching. Whereas dogs apparently outperform all other species so far tested, apes and monkeys have problems in using such cues. Since only mammalian species have been tested, information is lacking about the evolutionary origin of these abilities. We here present the first data on object-choice tasks conducted with an avian species, the common raven. Ravens are highly competitive scavengers, possessing sophisticated cognitive skills in protecting their food caches and pilfering others' caches. We conducted three experiments, exploring (i) which kind of cues ravens use for choosing a certain object, (ii) whether ravens use humans' gaze for detecting hidden food and (iii) whether ravens would find hidden food in the presence of an informed conspecific who potentially provides gaze cues. Our results indicate that ravens reliably respond to humans' touching of an object, but they hardly use point and gaze cues for their choices. Likewise, they do not perform above chance level in the presence of an informed conspecific. These findings mirror those obtained for primates and suggest that, although ravens may be aware of the gaze direction of humans and conspecifics, they apparently do not rely on this information to detect hidden food.

Enhanced social learning between siblings in common ravens, Corvus corax.

It has been suggested that social dynamics affect social learning but empirical support for this idea is scarce. Here we show that affiliate relationships among kin indeed enhance the performance of common ravens, Corvus corax, in a social learning task. Via daily behavioural protocols we first monitored social dynamics in our group of captive young ravens. Siblings spent significantly more time in close proximity to each other than did nonsiblings. We subsequently tested birds on a stimulus enhancement task in model-observer dyads composed of both siblings and nonsiblings. During demonstration the observer could watch the model manipulating one particular object (target object) in an adjacent room. After removing the model, the observer was confronted with five different objects including the former target object. Observers from sibling dyads handled the target object for significantly longer periods of time as compared with the other four available objects, whereas observers from nonsibling dyads did not show a preference for the target object. Also, siblings matched the model's decision to cache or not to cache objects significantly more often than did nonsiblings. Hence, siblings were likely to attend to both, the behaviour of the model (caching or noncaching) and object-specific details. Our results support the hypothesis that affiliate relations between individuals affect the transmission of information and may lead to directed social learning even when spatial proximity has been experimentally controlled for.

Corticosterone excretion patterns and affiliative behavior over development in ravens (Corvus corax).

Averse effects of social stress may be buffered by the presence of social allies, which mainly has been demonstrated in mammals and recently also in birds. However, effects of socio-positive behavior prior to fledging in relation to corticosterone excretion in altricial birds have not been investigated yet. We here monitored corticosterone excretion patterns in three groups of hand raised juvenile ravens (n=5, 6 and 11) in the nest, post-fledging (May-July) and when ravens would be independent from their parents (September-November). We related these corticosterone excretion patterns to socio-positive behavior. Behavioral data were collected via focal sampling in each developmental period considered. We analyzed amounts of excreted immunoreactive corticosterone metabolites (CM) using enzyme immuno assays. We collected fecal samples in each developmental period considered and evaluated the most appropriate assay via an isolation stress experiment. Basal CM was significantly higher during the nestling period than post-fledging or when birds were independent. The time nestlings spent allopreening correlated negatively with mean CM. Post-fledging, individuals with higher CM levels sat close to (distance <50 cm) conspecifics more frequently and tended to preen them longer. When birds were independent and a stable rank hierarchy was established, dominant individuals were preened significantly longer than subordinates. These patterns observed in ravens parallel those described for primates, which could indicate that animal species living in a complex social environment may deal with social problems in a similar way that is not restricted to mammals or primates.