Individuality in Problem Solving: String Pulling in Two Carduelis Species (Aves: Passeriformes)

The research reported here was designed to study the individual peculiarities of birds in solving a problem. Goldfinches Carduelis carduelis and siskins C. spinus were tested with the string‐pulling task: sitting on a perch from which a small food container is suspended by a string the test bird had to lift the container, using the bill to pull the string stepwise up and a foot to hold it, and repeat that until they could reach the food. Fifty‐two goldfinches and 29 siskins raised under controlled conditions were tested individually. Three groups became apparent: ‘inventors’ (23% of goldfinches; 62% of siskins) solved the problem by themselves; ‘imitators’ (25% of goldfinches; 10% of siskins) succeeded after seeing a performing conspecific; ‘duffers’ (52% of goldfinches, 28% of siskins) did not succeed either way. The species – but not the sexes – differed significantly in string‐pulling ability. The results of our experiments indicate that string pulling is an acquired combination of innate behaviour elements. An individual's string‐pulling competence may depend on prior experience of handling branchlets, on trial‐and‐error learning and on social learning (emulation). However, some individuals succeeded without these facilitating factors, while others did not succeed at all despite all of them present. Although functionally and motivationally related to feeding, the learned string pulling is often shown as a playful activity without an obvious reward.     

Blue-throated macaws (Ara glaucogularis) succeed in a cooperative task without coordinating their actions

Social complexity may select for socio-cognitive abilities. The “loose string” task has become a comparative benchmark paradigm for investigating cooperative problem-solving abilities in many species, thus enhancing our understanding of their evolution. It requires two individuals working together to solve a problem, specifically by pulling the two ends of a string simultaneously to move a reward towards them. A dyad's performance therefore depends on the individuals’ ability to coordinate their pulling action. Many species, including corvids and parrots, have been tested in this paradigm, but most appear insensitive to the exact cooperative nature of the task. We tested another parrot species, blue-throated macaws, to further our understanding of social cognition in psittacids. Five birds were tested with different partners in a dyadic setting. The study included two control conditions examining the cognitive mechanism underlying their seemingly cooperative behaviour. All birds were able to simultaneously pull the strings, but their performance did not drop when they were denied mutual visual access, and they failed to obtain food when they needed to wait for their partner. Moreover, the parrots decreased their latency to pull with increasing experience. These findings suggest that the birds may have applied an associatively learnt rule, or relied on acoustic cues, rather than coordinating their actions with the partner. This may not necessarily prove a lack of understanding the partner's role, given that their failure to wait in the delay control test might be explained by their poor inhibitory control abilities. Relationship quality (i.e. affiliation and food tolerance) did not influence dyadic success. Future studies are needed in order to disentangle macaws’ potentially limited cooperative abilities from their lack of inhibitory control.     

An Investigation into the Cognition Behind Spontaneous String Pulling in New Caledonian Crows

The ability of some bird species to pull up meat hung on a string is a famous example of spontaneous animal problem solving. The “insight” hypothesis claims that this complex behaviour is based on cognitive abilities such as mental scenario building and imagination. An operant conditioning account, in contrast, would claim that this spontaneity is due to each action in string pulling being reinforced by the meat moving closer and remaining closer to the bird on the perch. We presented experienced and naïve New Caledonian crows with a novel, visually restricted string-pulling problem that reduced the quality of visual feedback during string pulling. Experienced crows solved this problem with reduced efficiency and increased errors compared to their performance in standard string pulling. Naïve crows either failed or solved the problem by trial and error learning. However, when visual feedback was available via a mirror mounted next to the apparatus, two naïve crows were able to perform at the same level as the experienced group. Our results raise the possibility that spontaneous string pulling in New Caledonian crows may not be based on insight but on operant conditioning mediated by a perceptual-motor feedback cycle.     

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.     

String‐pulling behaviour in a Harris's Hawk Parabuteo unicinctus

Variations on the string‐pull experiment have been presented to a variety of avian species. Here, we present the results of a basic vertical string‐pull task with a Harris's Hawk Parabuteo unicinctus. A 2‐year‐old subject retrieved a shielded food reward within 8 min on each of eight trials and spontaneously used solving techniques similar to corvids and parrots. Our data contribute to the small body of literature on raptor cognition by showing that it may be within the realm of at least one bird of prey species to perform the string‐pull task similarly to avian species renowned for their high cognitive abilities.     

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.     

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.     

Social learning in common ravens, Corvus corax

We conducted an experiment to investigate whether the presence of a conspecific model can promote the acquisition of a motor task in common ravens. For this purpose, dyads, either of control birds or of model-observer pairings, were allowed to operate together in an arena with a set of identical boxes. Each box consisted of two compartments each containing a reward of three pieces of meat. The compartments were closed by gliding lids with red flaps on their front, opening horizontally in opposite directions. Naive control individuals opened the lids exclusively by levering, that is, jumping on top of the box, inserting the beak at the posterior rim of the lid and pushing it open. Models were trained to demonstrate an alternative opening technique, pulling at the front flap, then jumping on top of the box to get at the reward. In contrast to the control birds, observers initially opened boxes both ways, by pulling and levering. Furthermore, observers approached the boxes more quickly and showed less fearful behaviour than the control birds, which we attribute to the enhancing effect of the model. We discuss both stimulus enhancement and motor imitation as possible learning mechanisms. Even though observers initially obtained a considerable amount of reward produced by the models, scrounging evidently did not inhibit learning. Copyright 1999 The Association for the Study of Animal Behaviour.     

Experimental Manipulation of Food Accessibility Affects Conflict Management Behaviour in Ravens

Conflict management strategies such as reconciliation and bystander affiliation have been described for a variety of species. A common determinant seems to be a ‘complex’ social life, with individuals relying on affiliate relationships or social bonds. Little is known, however, about the strategic and flexible use of conflict management skills in experimental settings in species other than primates. We here investigated conflict and post‐conflict behaviour of ravens by manipulating the accessibility of food and, thus, the likelihood of aggressive interactions while foraging. Specifically, we presented birds with a certain amount of highly preferred food that varied in the number of pieces (one piece, two pieces or, as a control, small pieces matching the number of participating birds) and observed their agonistic behaviour during feeding and their affiliative behaviour afterwards. The results showed that high levels of conflicts during feeding in the 1‐piece and 2‐piece conditions led to high levels of affiliation after feeding. Depending on the experimental condition, this effect is best explained (a) by the affiliative behaviour of former aggressors (1‐piece condition) and (b) by the affiliation directed to the receivers of aggression after feeding (2‐piece condition). Those dyads that engaged in allo‐preening after feeding also engaged in allo‐preening outside the experimental setting, suggesting that socially bonded individuals provided third‐party affiliation to victims of aggression. Moreover, socially bonded ravens fed close to each other in the experiment when food was clumped, indicating that they actively coordinated their behaviour when there was a high conflict potential. Taken together, these findings support the assumption that ravens use their social bonds to avoid conflicts by choosing with whom to feed, and to buffer effects of conflicts by engaging in third‐party affiliation as post‐conflict behaviour.     

Food calling in wild ravens (Corvus corax) revisited: Who is addressed?

Numerous birds and mammals use vocal signals to advertise feeding opportunities but often such signals vary with individual and contextual factors. Non-breeding ravens call at food that is difficult to access, resulting in the attraction of nearby conspecifics. Although callers may benefit from group formation in various ways, we recently found substantial individual variation in food calling. We here explored whether this variation can be partly explained by the social dynamics in raven foraging groups, together with already known effects of age class and sex. Specifically, we expected ravens to respond to the presence or absence of affiliates that could act as cooperative partners in the forthcoming feeding event, that is they should call when other ravens were present but they themselves were alone rather than when they were also in company of an affiliation partner. We observed the vocal behaviour of individually marked wild ravens and, simultaneously, categorized their affiliative behaviour with other ravens in the minutes before experimentally controlled feedings. In line with our prediction, individuals were less likely to produce food-associated calls when they were in close contact with an affiliation partner prior to feeding as compared to when they were alone. Furthermore, sex and age class influenced food calling as females called more often than males and younger birds called more often than adult ravens. In conclusion, these results suggest that ravens attempt to find support from a particular cooperative partner by broadly advertise feeding opportunities via food-associated calls, especially when they have low chances in contest competition due to their age and sex. These findings lend further support to the assumption of raven flocks being structured by social relationships and individual birds flexibly controlling their vocal signalling according to the current flock composition.     

The portability of foodweb dynamics: reassembling an Australian eucalypt–psyllid–bird association within California

Aims To evaluate the role of native predators (birds) within an Australian foodweb (lerp psyllids and eucalyptus trees) reassembled in California. Location Eucalyptus groves within Santa Cruz, California. Methods We compared bird diversity and abundance between a eucalyptus grove infested with lerp psyllids and a grove that was uninfested, using point counts. We documented shifts in the foraging behaviour of birds between the groves using structured behavioural observations. Additionally, we judged the effect of bird foraging on lerp psyllid abundance using exclosure experiments. Results We found a greater richness and abundance of Californian birds within a psyllid infested eucalyptus grove compared to a matched non‐infested grove, and that Californian birds modify their foraging behaviour within the infested grove in order to concentrate on ingesting psyllids. This suggests that Californian birds could provide indirect top‐down benefits to eucalyptus trees similar to those observed in Australia. However, using bird exclosure experiments, we found no evidence of top‐down control of lerp psyllids by Californian birds. Main conclusions We suggest that physiological and foraging differences between Californian and Australian pysllid‐eating birds account for the failure to observe top‐down control of psyllid populations in California. The increasing rate of non‐indigenous species invasions has produced local biotas that are almost entirely composed of non‐indigenous species. This example illustrates the complex nature of cosmopolitan native‐exotic food webs, and the ecological insights obtainable through their study.     

Patterned-String Tasks: Relation between Fine Motor Skills and Visual-Spatial Abilities in Parrots

String-pulling and patterned-string tasks are often used to analyse perceptual and cognitive abilities in animals. In addition, the paradigm can be used to test the interrelation between visual-spatial and motor performance. Two Australian parrot species, the galah (Eolophus roseicapilla) and the cockatiel (Nymphicus hollandicus), forage on the ground, but only the galah uses its feet to manipulate food. I used a set of string pulling and patterned-string tasks to test whether usage of the feet during foraging is a prerequisite for solving the vertical string pulling problem. Indeed, the two species used techniques that clearly differed in the extent of beak-foot coordination but did not differ in terms of their success in solving the string pulling task. However, when the visual-spatial skills of the subjects were tested, the galahs outperformed the cockatiels. This supports the hypothesis that the fine motor skills needed for advanced beak-foot coordination may be interrelated with certain visual-spatial abilities needed for solving patterned-string tasks. This pattern was also found within each of the two species on the individual level: higher motor abilities positively correlated with performance in patterned-string tasks. This is the first evidence of an interrelation between visual-spatial and motor abilities in non-mammalian animals.     

Ravens, Corvus corax, differentiate between knowledgeable and ignorant competitors

Human social behaviour is influenced by attributing mental states to others. It is debated whether and to what extent such skills might occur in non-human animals. We here test for the possibility of ravens attributing knowledge about the location of food to potential competitors. In our experiments, we capitalize on the mutually antagonistic interactions that occur in these birds between those individuals that store food versus those that try to pilfer these caches. Since ravens' pilfer success depends on memory of observed caches, we manipulated the view of birds at caching, thereby designing competitors who were either knowledgeable or ignorant of cache location and then tested the responses of both storers and pilferers to those competitors at recovery. We show that ravens modify their cache protection and pilfer tactics not simply in response to the immediate behaviour of competitors, but also in relation to whether or not they previously had the opportunity of observing caching. Our results suggest that the birds not only recall whom they had seen during caching, but also know that obstacles can obstruct the view of others and that this affects pilfering.     

Effects of Group Size on Approach to Novel Objects in Ravens (Corvus corax)

Neophobia may constrain explorative behaviour, learning and innovation, while social context may facilitate approach to novel objects and acceptance of novel food. We examined the effects of neophobia on the exploration of novel objects in relation to social context in ravens (Corvus corax). Ravens are suitable subjects for studying effects of social context, as they are highly neophobic scavengers that recruit conspecifics to food. We tested two groups of six and 11 hand‐raised birds in three conditions: single‐bird, in dyadic combinations and sibling sub‐groups of three to six birds. Contrary to expectation, individuals of both groups were quicker to approach novel objects when tested alone than when tested with conspecifics. However, they spent more time close to and manipulating the novel objects in the social conditions (dyadic and group) than when being alone. We discuss the possibility that the higher latencies of dyads and groups to approach novel objects may reflect a ‘negotiation’ process in a ‘war of attrition’ between the individuals over risk‐taking.     

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. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 870–877.     

Individual and social factors affecting the ability of American crows to solve and master a string pulling task

Crows and other birds in the family Corvidae regularly share information to learn the identity and whereabouts of dangerous predators, but can they use social learning to solve a novel task for a food reward? Here, we examined the factors affecting the ability of 27 wild-caught American crows to solve a common string pulling task in a laboratory setting. We split crows into two groups; one group was given the task after repeatedly observing a conspecific model the solution and the other solved in the absence of conspecific models. We recorded the crows’ estimated age, sex, size, body condition, level of nervousness, and brain volume using DICOM images from a CT scan. Although none of these variables were statistically significant, crows without a conspecific model and large brain volumes consistently mastered the task in the minimum number of days, whereas those with conspecific models and smaller brain volumes required varying and sometimes a substantial number of days to master the task. We found indirect evidence that body condition might also be important for motivating crows to solve the task. Crows with conspecific models were no more likely to initially solve the task than those working the puzzle without social information, but those that mastered the task usually copied the method most frequently demonstrated by their knowledgeable neighbors. These findings suggest that brain volume and possibly body condition may be factors in learning new tasks and that crows can use social learning to refine their ability to obtain a novel food source, although they must initially learn to access it themselves.     

Corvids congregate to breeding colonies of a burrow‐nesting seabird

Egg predation is a major cause of reproductive failure among birds, and can compromise the viability of affected populations. Some egg predators aggregate near colonially breeding birds to exploit the seasonal increase of prey resources. We investigated spatial and temporal variations in the abundance of an egg predator (little raven Corvus mellori; Corvidae) to identify whether ravens aggregate spatially or temporally to coincide with any of three potential prey species: burrow‐nesting little penguin (Eudyptula minor; Spheniscidae), short‐tailed shearwater (Ardenna tenuirostris; Procellariidae), and surface‐nesting silver gull (Chroicocephalus novaehollandiae; Laridae). We derived spatially explicit density estimates of little ravens using distance sampling along line transects throughout a calendar year, which encompassed little penguin, short‐tailed shearwater and silver gull breeding and non‐breeding seasons. High raven abundance coincided temporally with penguin and gull egg laying periods but not with that of shearwaters. The spatial distribution of raven density corresponded with the little penguin colony but not with shearwater or gull colonies. Thus, the presence of little penguin eggs in burrows correlated strongly with little raven activity, and this implies that little ravens may have learnt to exploit the plentiful subsurface food resource of little penguin eggs. Corvid management may be required to maintain the viability of this socially and economically important penguin colony.     

Scrounging Tactics in Free-Ranging Ravens, Corvus corax

Social foraging allows individuals to scrounge, i.e. to exploit the food others have made available. The conditions promoting scrounging as an alternative foraging tactic have yet received limited attention. We presently examine whether ravens, as opportunistic scavengers, adjust their foraging tactics according to the potential costs involved in accessing a particular food source. We observed wild ravens foraging in a game park, at the enclosures of wolves, Canis lupus, and wild boars, Sus scrofa. Wolves may aggressively defend their food and even kill ravens, whereas wild boars do not. When co‐feeding with wolves, the ravens showed higher scrounging rates than with wild boars. Only at the wolves, they tended to specialize either on scrounging or on getting food directly from the site. However, scrounging techniques differed in relation to the state of food depletion. Early on, after food became available, the ravens most frequently displaced others from food, whereas towards the end, stealing, solicited sharing, and cache raiding became prevalent. These techniques differed in their profitability and their use was related to the scroungers’ age, social status and affiliative relationships. This suggests that ecological conditions, such as co‐feeding with potential predators, may influence the individuals’ decision whether or not to scrounge in competition for food. Social conditions, on the other hand, may affect the way how to get at food possessed by others and may thus, to a large extent, determine the profitability of scrounging.     

An end to insight? New Caledonian crows can spontaneously solve problems without planning their actions

Animals rarely solve problems spontaneously. Some bird species, however, can immediately find a solution to the string-pulling problem. They are able to rapidly gain access to food hung on the end of a long string by repeatedly pulling and then stepping on the string. It is currently unclear whether these spontaneous solutions are produced by insight or by a perceptual-motor feedback loop. Here, we presented New Caledonian crows and humans with a novel horizontal string-pulling task. While the humans succeeded, no individual crow showed a significant preference for the connected string, and all but one failed to gain the food even once. These results clearly show that string pulling in New Caledonian crows is generated not by insight, but by perceptual feedback. Animals can spontaneously solve problems without planning their actions.     

A test of imitative learning in starlings using a two-action method with an enhanced ghost control

Imitative learning, in which an individual learns to reproduce the behaviour pattern of another, has attracted considerable attention as a potentially powerful form of social learning. Despite extensive research, however, it has proved difficult to demonstrate in nonhuman animals. We investigated the ability of European starlings, Sturnus vulgaris, to imitate the behaviour of a conspecific. Subjects watched a trained conspecific manipulating a plug for access to a food reward, using either a pushing or a pulling action. When later tested with the same apparatus these birds completed the task using the same action they had previously observed. In a second experiment, a separate group of starlings saw the plug move upwards or downwards automatically and a nearby conspecific obtain a food reward. When given access to the task these starlings failed to move the plug in the direction they had seen. Our experiment is an improvement on previous bidirectional control designs and provides strong evidence that starlings are capable of imitation. We advocate further use of this experimental design in attempts to demonstrate imitative learning. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.