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.     

Relative numerousness judgements in crows and pigeons in the urgent comparison of stimuli earlier linked to different amounts of reinforcement]

The ability of pigeons (Colomba livia, L.) and crows (Corvus corone cornix, L.) was studied to realize urgent numerousness judgement of reinforcement consisting of discrete elements (wheat grains and meal worm larvae, respectively). In the process of preliminary training the birds mastered the information about the conformity of the feeder colour with the definite number (1-9 for pigeons and 5-12 for crows) of reinforcement units at isolated presentation of feeders. In test at presentation of pairs formed from these feeders, pigeons and crows chose the stimulus connected with a greater quantity of reinforcement. In the range of 1-8 units the precision of choice in pigeons depended on absolute and relative differences between comparing values. In crows in the range of 6-12 this dependence was not revealed. The ability to solve the given test is considered as one of manifestations of elementary reasoning.     

Lateralized tool use in wild New Caledonian crows

Many vertebrate species exhibit sensory and motor asymmetries. Laterality studies of tool use have focused on primates, where hemispheric asymmetries, manifested behaviourally in hand preferences, are thought to be associated with complex motor tasks. Here we report strong individual lateralization for tool use in birds. New Caledonian crows, Corvus moneduloides, hold stick tools with their bills while foraging, often with the nonworking end laterally positioned on one side of the head and the working end possibly positioned in the binocular field. We observed four wild crows to determine whether tools were consistently held on one side. All crows showed a significant preference (two right, two left). This preference was independent of any asymmetry in tool manufacture and held for artificial holes similarly accessible for tools held on either side. This is the first demonstration of lateralized tool use in a nonprimate. In addition, all 173 tools used unilaterally were held only on a crow's preferred side. Such pronounced individual laterality for tool use in natural conditions has previously been reported only in humans and chimpanzees.     

Conditioning of gray crows (Corvus cornix L.) in a "giant" eight-arm radial maze

Twelve adult hooded crows (Corvus cornix) were trained to perform a standard radial-maze task in a giant eight-arm outdoor radial maze constructed at the "Chistyi les" Biological Station (Tver oblast) for comparative investigations of spatial memory in birds and mammals. The maze consists of a central part of 250 cm diameter, and has arms of 650 cm length, 170 cm height and 80 cm width. The examined hooded crows showed good task performance. Errors (repeated visits to empty arms) were few in number and were predominantly connected with the tendency to avoid arms close to an observer.     

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.     

Evaluation of the ability to solve the Revecz-Krushinski? test in corvine birds

Reasoning ability in crows was investigated by means of the Revecz-Krushinski? test, in which the bird has to apprehend the rule of stimulus (food bait) displacement: "In each next trial the food bait is hidden in a new place--one step further along the row". By means of computer modelling the criteria of statistical evaluation of this problem solving were established. The test was considered solved when the number of trials which preceded the detection of food was less than those which were calculated for chance performance. High level of reasoning ability in crows is discussed.     

Do New Caledonian crows solve physical problems through causal reasoning?

The extent to which animals other than humans can reason about physical problems is contentious. The benchmark test for this ability has been the trap-tube task. We presented New Caledonian crows with a series of two-trap versions of this problem. Three out of six crows solved the initial trap-tube. These crows continued to avoid the trap when the arbitrary features that had previously been associated with successful performances were removed. However, they did not avoid the trap when a hole and a functional trap were in the tube. In contrast to a recent primate study, the three crows then solved a causally equivalent but visually distinct problem--the trap-table task. The performance of the three crows across the four transfers made explanations based on chance, associative learning, visual and tactile generalization, and previous dispositions unlikely. Our findings suggest that New Caledonian crows can solve complex physical problems by reasoning both causally and analogically about causal relations. Causal and analogical reasoning may form the basis of the New Caledonian crow's exceptional tool skills.     

Visual coverage and scanning behavior in two corvid species: American crow and Western scrub jay

Inter-specific differences in the configuration of avian visual fields and degree of eye/head movements have been associated with foraging and anti-predator behaviors. Our goal was to study visual fields, eye movements, and head movements in two species of corvids: American crow (Corvus brachyrhynchos) and Western scrub jay (Aphelocoma californica). American crows had wider binocular overlap, longer vertical binocular fields, narrower blind areas, and higher amplitude of eye movement than Western scrub jays. American crows can converge their eyes and see their own bill tip, which may facilitate using different foraging techniques (e.g., pecking, probing) and manufacturing and handing rudimentary tools. Western scrub jays had a higher head movement rate than American crows while on the ground, and the opposite between-species difference was found when individuals were perching. Faster head movements may enhance the ability to scan the environment, which may be related to a higher perceived risk of predation of Western scrub jays when on the ground, and American crows when perching. The visual field configuration of these species appears influenced mostly by foraging techniques while their scaning behavior, by predation risk.     

Spontaneous metatool use by New Caledonian crows

A crucial stage in hominin evolution was the development of metatool use -- the ability to use one tool on another [1, 2]. Although the great apes can solve metatool tasks [3, 4], monkeys have been less successful [5-7]. Here we provide experimental evidence that New Caledonian crows can spontaneously solve a demanding metatool task in which a short tool is used to extract a longer tool that can then be used to obtain meat. Six out of the seven crows initially attempted to extract the long tool with the short tool. Four successfully obtained meat on the first trial. The experiments revealed that the crows did not solve the metatool task by trial-and-error learning during the task or through a previously learned rule. The sophisticated physical cognition shown appears to have been based on analogical reasoning. The ability to reason analogically may explain the exceptional tool-manufacturing skills of New Caledonian crows.     

Brains, tools, innovation and biogeography in crows and ravens

ABSTRACT: BACKGROUND: Crows and ravens (Passeriformes: Corvus) are large-brained birds with enhanced cognitive abilities relative to other birds. They are among the few non-hominid organisms on Earth to be considered intelligent and well-known examples exist of several crow species having evolved innovative strategies and even use of tools in their search for food. The 40 Corvus species have also been successful dispersers and are distributed on most continents and in remote archipelagos. RESULTS: This study presents the first molecular phylogeny including all species and a number of subspecies within the genus Corvus. We date the phylogeny and determine ancestral areas to investigate historical biogeographical patterns of the crows. Additionally, we use data on brain size and a large database on innovative behaviour and tool use to test whether brain size (i) explains innovative behaviour and success in applying tools when foraging and (ii) has some correlative role in the success of colonization of islands. Our results demonstrate that crows originated in the Palaearctic in the Miocene from where they dispersed to North America and the Caribbean, Africa and Australasia. We find that relative brain size alone does not explain tool use, innovative feeding strategies and dispersal success within crows. CONCLUSIONS: Our study supports monophyly of the genus Corvus and further demonstrates the direction and timing of colonization from the area of origin in the Palaearctic to other continents and archipelagos. The Caribbean was probably colonized from North America, although some North American ancestor may have gone extinct, and the Pacific was colonized multiple times from Asia and Australia. We did not find a correlation between relative brain size, tool use, innovative feeding strategies and dispersal success. Hence, we propose that all crows and ravens have relatively large brains compared to other birds and thus the potential to be innovative if conditions and circumstances are right.     

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.     

Fast exact algorithms for the closest string and substring problems with application to the planted (L, d)-motif model

We present two parameterized algorithms for the closest string problem. The first runs in O(nL + nd · 17.97d) time for DNA strings and in O(nL + nd · 61.86d) time for protein strings, where n is the number of input strings, L is the length of each input string, and d is the given upper bound on the number of mismatches between the center string and each input string. The second runs in O(nL + nd · 13.92d) time for DNA strings and in O(nL + nd · 47.21d) time for protein strings. We then extend the first algorithm to a new parameterized algorithm for the closest substring problem that runs in O((n - 1)m2(L + d · 17.97d · m[log2(d+1)])) time for DNA strings and in O((n - 1)m2(L + d · 61.86d · m[log2(d+1)])) time for protein strings, where n is the number of input strings, L is the length of the center substring, L - 1 + m is the maximum length of a single input string, and d is the given upper bound on the number of mismatches between the center substring and at least one substring of each input string. All the algorithms significantly improve the previous bests. To verify experimentally the theoretical improvements in the time complexity, we implement our algorithm in C and apply the resulting program to the planted (L, d)-motif problem proposed by Pevzner and Sze in 2000. We compare our program with the previously best exact program for the problem, namely PMSPrune (designed by Davila et al. in 2007). Our experimental data show that our program runs faster for practical cases and also for several challenging cases. Our algorithm uses less memory too.     

Context-dependent tool use in New Caledonian crows

Humans and chimpanzees both exhibit context-dependent tool use. That is, both species choose to use tools when food is within reach, but the context is potentially hazardous. Here, we show that New Caledonian crows used tools more frequently when food was positioned next to a novel model snake than when food was positioned next to a novel teddy bear or a familiar food bowl. However, the crows showed no significant difference in their neophobic reactions towards the teddy bear and the model snake. Therefore, the crows used tools more in response to a risky object resembling a natural predator than to a less-threatening object that provoked a comparable level of neophobia. These results show that New Caledonian crows, like humans and chimpanzees, are capable of context-dependent tool use.     

Cognitive abilities related to tool use in the woodpecker finch, Cactospiza pallida

Woodpecker finches are famous for their spontaneous tool use behaviour in the wild. They use twigs or cactus spines to pry arthropods out of crevices and use this ability more than any other tool-using species known. We experimentally investigated the cognitive abilities related to tool use. We chose three experimental designs that have been used to test several primate species (trap tube task and modification task) and New Caledonian crows (tool length task). One of six woodpecker finches was able to solve the trap tube task, and several individuals modified tools and chose twigs of appropriate length. Most subjects mastered these new tasks quickly, but we found no evidence that they were able to assess the problems in advance. These findings resemble those obtained for primates in these tasks.     

Mesopredators constrain a top predator: competitive release of ravens after culling crows

Although predator control programmes rarely consider complex competitive interactions among predators, it is becoming clear that removal of larger ‘superior’ competitors often releases the ‘inferior’ ones and can precipitate trophic cascades. In contrast, our study indicates that culling hooded crows Corvus cornix appears to release a larger competitor, the common raven Corvus corax. Ravens ranged more widely, and the predation of artificial nests was significantly faster (although total predation was similar), after the removal of crows. Our study provides evidence of a novel reversal of competitive release where a larger species was freed from constraints imposed on its distribution and behaviour by a smaller species, and emphasizes the importance of considering community and ecosystem effects of predator manipulations when undertaken for conservation or game management.     

Extra‐pair paternity as a strategy to reduce the costs of heterospecific reproduction? Insights from the crow hybrid zone

Within hybrid zones of socially monogamous species, the number of mating opportunities with a conspecific can be limited. As a consequence, individuals may mate with a heterospecific (social) partner despite possible fitness costs to their hybrid offspring. Extra‐pair copulations with a conspecific may thus arise as a possible post hoc strategy to reduce the costs of hybridization. We here assessed the rate of extra‐pair paternity in the hybrid zone between all‐black carrion crows (Corvus (corone) corone) and grey hooded crows (C. (c.) cornix) and tested whether extra‐pair paternity (EPP) was more likely in broods where parents differed in plumage colour. The proportion of broods with at least one extra‐pair offspring and the proportion of extra‐pair offspring were low overall (6.98% and 2.90%, respectively) with no evidence of hybrid broods having higher EPP rates than purebred nests.     

Social learning spreads knowledge about dangerous humans among American crows

Individuals face evolutionary trade-offs between the acquisition of costly but accurate information gained firsthand and the use of inexpensive but possibly less reliable social information. American crows (Corvus brachyrhynchos) use both sources of information to learn the facial features of a dangerous person. We exposed wild crows to a novel 'dangerous face' by wearing a unique mask as we trapped, banded and released 7-15 birds at five study sites near Seattle, WA, USA. An immediate scolding response to the dangerous mask after trapping by previously captured crows demonstrates individual learning, while an immediate response by crows that were not captured probably represents conditioning to the trapping scene by the mob of birds that assembled during the capture. Later recognition of dangerous masks by lone crows that were never captured is consistent with horizontal social learning. Independent scolding by young crows, whose parents had conditioned them to scold the dangerous mask, demonstrates vertical social learning. Crows that directly experienced trapping later discriminated among dangerous and neutral masks more precisely than did crows that learned through social means. Learning enabled scolding to double in frequency and spread at least 1.2 km from the place of origin over a 5 year period at one site.     

Testing Problem Solving in Ravens: String-Pulling to Reach Food

The aim of our study was to re‐examine the acquisition of problem‐solving behaviour in ravens: accessing meat suspended from a perch by a string. In contrast to a previous study, here we: (i) controlled for possible effects of fear of the string, competition by dominants, and social learning and (ii) devised a mechanically equivalent but non‐intuitive task to test for the possibility of means–end understanding. One‐year‐old ravens confronted with meat on a string for the first time tried several ways to reach the food. However, five of six birds suddenly performed a coherent sequence of pulling up and stepping on loops of string, essential for solving the problem. Those five birds were also successful in the non‐intuitive task where they had to pull down the string to lift the meat. A second group of birds with similar exposure to strings but without any experience in pulling up meat failed the pull‐down test. These results support the idea that the ravens’ behaviour in accessing meat on a string is not only a product of rapid learning but may involve some understanding of cause–effect relation between string, food and certain body parts.     

Crows cross-modally recognize group members but not non-group members

Recognizing other individuals by integrating different sensory modalities is a crucial ability of social animals, including humans. Although cross-modal individual recognition has been demonstrated in mammals, the extent of its use by birds remains unknown. Herein, we report the first evidence of cross-modal recognition of group members by a highly social bird, the large-billed crow (Corvus macrorhynchos). A cross-modal expectancy violation paradigm was used to test whether crows were sensitive to identity congruence between visual presentation of a group member and the subsequent playback of a contact call. Crows looked more rapidly and for a longer duration when the visual and auditory stimuli were incongruent than when congruent. Moreover, these responses were not observed with non-group member stimuli. These results indicate that crows spontaneously associate visual and auditory information of group members but not of non-group members, which is a demonstration of cross-modal audiovisual recognition of group members in birds.     

Cognitive Processes Associated with Sequential Tool Use in New Caledonian Crows

Background

Using tools to act on non-food objects—for example, to make other tools—is considered to be a hallmark of human intelligence, and may have been a crucial step in our evolution. One form of this behaviour, ‘sequential tool use’, has been observed in a number of non-human primates and even in one bird, the New Caledonian crow (Corvus moneduloides). While sequential tool use has often been interpreted as evidence for advanced cognitive abilities, such as planning and analogical reasoning, the behaviour itself can be underpinned by a range of different cognitive mechanisms, which have never been explicitly examined. Here, we present experiments that not only demonstrate new tool-using capabilities in New Caledonian crows, but allow examination of the extent to which crows understand the physical interactions involved.

Methodology/Principal Findings

In two experiments, we tested seven captive New Caledonian crows in six tasks requiring the use of up to three different tools in a sequence to retrieve food. Our study incorporated several novel features: (i) we tested crows on a three-tool problem (subjects were required to use a tool to retrieve a second tool, then use the second tool to retrieve a third one, and finally use the third one to reach for food); (ii) we presented tasks of different complexity in random rather than progressive order; (iii) we included a number of control conditions to test whether tool retrieval was goal-directed; and (iv) we manipulated the subjects'' pre-testing experience. Five subjects successfully used tools in a sequence (four from their first trial), and four subjects repeatedly solved the three-tool condition. Sequential tool use did not require, but was enhanced by, pre-training on each element in the sequence (‘chaining’), an explanation that could not be ruled out in earlier studies. By analyzing tool choice, tool swapping and improvement over time, we show that successful subjects did not use a random probing strategy. However, we find no firm evidence to support previous claims that sequential tool use demonstrates analogical reasoning or human-like planning.

Conclusions/Significance

While the ability of subjects to use three tools in sequence reveals a competence beyond that observed in any other species, our study also emphasises the importance of parsimony in comparative cognitive science: seemingly intelligent behaviour can be achieved without the involvement of high-level mental faculties, and detailed analyses are necessary before accepting claims for complex cognitive abilities.