The social life of corvids
Nicola S. Clayton1, and Nathan J. Emery2,1Department of Experimental Psychology, University of Cambridge, Cambridge CB2 3EB, UK
2Sub-department of Animal Behaviour, University of Cambridge, Cambridge CB3 8AA, UK
Available online 20 August 2007.
Of the 120 species of birds in the corvid family, which includes the crows, ravens, magpies and jays, the bare-faced rook is perhaps the most social of them all. At a rookery in Norfolk, for example, winter roosts can number up to 60,000 individuals. The name for a congregation of rooks is a ‘parliament’. In English folklore, parliament is an apt name for rook justice, as it is said that rooks form a circle around a wrongdoer producing a cacophony of calls and caws which can go on for hours until the offender is either attacked and killed or released to live another day. Although only fiction, such tales reflect their canny reputation as thieves and tricksters, as well as possessors of great wisdom.
Like most birds, corvids are monogamous, and the core unit is therefore the mated pair. This pair bond is typically for life, and the pair remains together throughout the year. For example, rooks and ravens find a partner during the autumn months, taking part in impressive aerobatic displays and food sharing which may be to assess the quality of a potential mate. Once juvenile rooks and ravens pair, they engage in extensive mutual preening and bill twining (bill holding) and support one another in fights.
Spontaneous Metatool Use by New Caledonian Crows
Alex H. Taylor1, , , Gavin R. Hunt1, Jennifer C. Holzhaider1 and Russell D. Gray1, , 1Department of Psychology, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
Received 27 June 2007;
revised 24 July 2007;
accepted 25 July 2007.
Published online: August 16, 2007.
Available online 16 August 2007.
A crucial stage in hominin evolution was the development of metatool use—the ability to use one tool on another  and . Although the great apes can solve metatool tasks  and , monkeys have been less successful ,  and . 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.
Results and Discussion
Metatool use was one of the major innovations in human evolution  and . The use of simple stone tools to make more complex tools may reflect the “cognitive leap” that initiated technological evolution in hominins . Metatool use has three distinct cognitive challenges. First, an individual must recognize that tools can be used on nonfood objects. This recognition may require analogical reasoning abilities . Second, an individual must initially inhibit a direct response toward the main goal of obtaining food, a reaction that both children and primates find difficult to suppress ,  and . Third, an individual must be capable of hierarchically organized behavior  and . That is, they must be able to flexibly integrate newly innovated behavior (tool→tool) with established behaviors as a subgoal in achieving a main goal (tool→tool→food). Such flexible, hierarchical organization of behavior has been suggested to follow a recursive pattern and to require cognitive processing similar to language production .
In early hominins, the transfer of a thrusting percussion technique from breaking nuts to knapping cutting tools was likely part of longer behavioral sequences in which tool materials and food were acquired separately . Metatool use, therefore, probably involved considerable behavioral organization in space and time. Tests for metatool use in great apes and monkeys have typically followed an experimental design where a small stick can be used to retrieve a nearby longer stick that can then be used to gain otherwise inaccessible food. The close proximity of the tools and the food in these tests eliminates tool transport and facilitates assessment of the relevant requirements of the task. It also makes it relatively easy to accidentally touch the long tool with the short tool in normal exploratory behavior, and thereby chance upon the solution. Increased distance between tools and the food source has been suggested to increase the cognitive demands of a tool task  and .Striking evidence is now emerging that Corvidae have convergently evolved cognitive abilities that rival those of our primate relatives . Evidence for convergent evolution include the impressive tool-manufacturing skills of New Caledonian crows (Corvus moneduloides) , , , ,  and  and complex physical cognition in non-tool-using rooks (Corvus frugilegus) . To test whether New Caledonian crows (crows hereafter) are capable of metatool use, we used an experimental design similar to the standard design used with great apes  and . We modified the design to give a greater degree of spatial and temporal separation between the tools and the food. In our experiments, food (meat) was placed in a 15 cm deep horizontal hole 1.75 m away from two identical “toolboxes” (Figure 1). The front of each toolbox consisted of vertical bars that allowed a crow to insert its bill but not its head. We placed an 18 cm long stick tool 4 cm inside one toolbox. This tool was long enough to extract the meat but out of reach of a crow's bill. In the other toolbox, we placed a stone in a similar position. The positions of the stone and tool were randomized between the toolboxes across trials. Presenting both a relevant and an irrelevant object controlled for random probing of the toolboxes leading to a solution by trial and error. In front of the toolboxes, we placed a 5 cm long tool (Figure 1). This tool was too short to extract the meat but could be used to extract the long tool from the tool box. Successful completion of the task required a crow to use the short stick to extract the long stick from the box and then transport the long stick to the hole and extract the food.The experimental apparatus consists of a long, functional tool in one toolbox, a stone in the second toolbox, a short, nonfunctional tool in front of both toolboxes, and a 15 cm deep horizontal hole in which meat was placed. The distance between the hole and the toolboxes was 1.75 m but is reduced in the image to save space.
All seven crows developed metatool use and extracted the food (Figure 2). Icarus, Luigi, and Gypsy spontaneously produced the correct behavioral sequence in the first trial (Gypsy's and Icarus's first trial are shown in Movies S1 and S2, respectively, in the Supplemental Data available online). This was despite the requirement to transport tools and the difficulty in obtaining a tool from behind the bars. Joker also successfully solved the problem on the first trial, but made the error of taking the short tool to the hole after a first attempt at extracting the long stick (Figure 2). Colin, Lucy, and Ruby first extracted food in the 5th, 19th, and 23rd trial, respectively. Significantly, the first use of the short stick by six of the seven crows was either successful metatool use or a failed attempt to extract the long tool. This performance is comparable with that of the great apes  and . In the first trial, five out of six gorillas and three out of five orangutans used a tool as a metatool . However, only three out of five chimpanzees (Pan troglodytes) developed metatool use, and these individuals first made the error of attempting to use the small, nonfunctional stick tool to obtain the food . Monkeys have been less successful. One out of two capuchins (Cebus apella) performed at a similar level to gorillas and developed metatool use on the first trial . In another study, only one out of six capuchins used tools as metatools and this individual succeeded in less than 50% of trials . Despite receiving considerable training on tool use, Japanese macaques (Macaca fuscata) did not attempt metatool use on the first trial and required more than 50 trials to achieve a 75% success rate .
Initial use of the nonfunctional tool in an attempt to get the food frequently occurs in primate metatool-use studies  and . In our experiment, only Lucy made the error of first taking the nonfunctional stick to the hole. Four crows (Ruby, Joker, Luigi, and Colin) occasionally attempted to use the nonfunctional tool to get food in later trials, but only after unsuccessfully trying to extract the long tool with the short tool. These crows appeared to have had difficulty extracting the long tool from the barred toolbox. They may have then taken the nonfunctional short tool to the hole because of problems inhibiting tool use when no other course of action was available.
The task could have been solved by trial-and-error learning if crows had initially used tool-related exploratory behavior toward the toolboxes and stumbled across the solution. However, the crows did not randomly probe the toolboxes. The first toolbox probed by all seven crows was the one with the long stick rather than the stone. In fact, only Ruby ever probed the toolbox containing the stone; she did so once, several trials after successful metatool use. This suggests that metatool use did not develop through trial-and-error learning during the experiment. The use of a previously learned behavioral rule by the crows is also unlikely. Familiarization training with the apparatus did not involve metatool use, and we have never seen this behavior in the wild in more than 3 years of observing crows on Maré. The spontaneous development of metatool use therefore required cognition more complex than simple learning mechanisms.
One possibility is that the crows solved the metatool task by analogical reasoning. Successfully constructing an analogy requires that an individual maps experience from previous problems onto a structurally similar, novel problem ,  and . One language-trained chimpanzee has been reported to have solved both figural and conceptual analogy problems . The crows may have solved the metatool-use task by perceiving the shared causal relationship between the task and normal tool use, namely that a tool can access out of reach objects. Children's performance with causal analogies depends in part on knowledge of the relevant causal properties of the task ,  and . Causal understanding is indicated by the spontaneous correction of mistakes in an appropriate, goal-directed way  and . If the crows had understood the relevant causal relationship in this experiment, we would expect them to use this knowledge to avoid making errors based on tool type.
To see whether crows were sensitive to the causal aspects of the food extraction task, we carried out a second experiment where the positions of the short and long tools were reversed. The long tool was now freely available so that metatool use was not required to extract the food. In the first block of five trials, all six crows tested initially inserted the long tool into the toolbox containing the short tool, but this generally occurred in the first block of five trials (Figure 3). This behavior usually lasted momentarily and there was often no contact with the short tool. In the only exception, Lucy extracted the short stick from the toolbox in her first trial but did not take it to the hole. No crow took the short stick to the hole. The insertion of the long tool appeared to be due to the difficulties in deviating from habitual behavior . The crows may have routinely probed the toolbox with the long tool because they had been rewarded in the previous ten metatool-use trials for probing the box. The crows rapidly rectified this mistake, suggesting that they were sensitive to the causal relationship between the tools and the final goal.
Our findings provide experimental evidence that New Caledonian crows can spontaneously solve a metatool task. On their first attempt to solve the problem, six out of seven crows used the short tool to probe the toolbox with the long tool. This appropriate spontaneous behavior and the quick correction of causal errors suggest that the crows used analogical reasoning to solve the metatool task. Analogical reasoning may be the crucial factor in the exceptional tool-manufacturing skills of New Caledonian crows.
We carried out the experiments with seven wild New Caledonian crows captured on Maré Island, New Caledonia. We housed up to three crows at a time in a 2-cage outdoor aviary at the location of capture; each cage was 4 m × 2 m × 3 m high. After capture, a crow was left to get accustomed to the aviary and human presence for 3 days before the experimental procedures began. During the experimental work, crows were held in one cage and the experimental apparatus was in the second cage; crows could not see between the cages. All crows were released at their site of capture after the experiment.
Each crow was given 10 familiarization trials in each of the following tasks before testing began: (1) extracting meat from the 15 cm deep horizontal hole with an 18 cm long stick that we provided; (2) withdrawing an 18 cm long stick from the toolbox and extracting meat from the hole (one end of the stick extended out between the bars, making it easy for crows to see and extract it); and (3) using a nonfunctional 5 cm long stick to try and extract meat from the 15 cm deep hole. The familiarization trials were carried out in blocks of five, in the following sequence: (1), (2), (3), (1), (2), and (3).
Before the first trial in the testing phase, each crow was given a 5 min familiarization period with the experimental setup without the short tool present. The short tool was placed in front of the toolboxes at the start of all trials. The trials were 10 min long and in blocks of five. To ensure that birds were exposed to the problem for standardized blocks of time, the position of the short stick was reset if a bird moved and then discarded it before the 10 min trial period ended. Testing continued until a crow had solved the task in 80% of trials across two consecutive 5-trial blocks or until 35 trials had been completed.
The authors thank W. Wardrobert and his family for access to their land. This work was supported by a Commonwealth Doctoral Scholarship (to A.H.T.) and a grant from the New Zealand Marsden Fund (to G.R.H. and R.D.G.). We are grateful to M. Corballis for helpful advice about the methodology and V. Ward for drawing Figure 1. Our work was carried out under University of Auckland Animal Ethics Committee approval R375.
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Movie S1. Gypsy's Successful First Metatool-Use Trial. This movie shows Gypsy's successful first metatool-use trial (see Block 1: Trial 1 in Figure 2). Gypsy picks up the short, nonfunctional tool in front of the two toolboxes and immediately uses it to extract the long, functional tool. Gypsy then extracts the meat with the long tool.
Movie S2. Icarus's Successful First Metatool-Use Trial. This movie shows Icarus's successful first metatool-use trial (see Block 1: Trial 1 in Figure 2). Icarus picks up the short, nonfunctional tool in front of the two toolboxes and immediately uses it to extract the long, functional tool. Icarus then extracts the meat with the long tool.
aDepartment of Experimental Psychology and Sub-department of Animal Behaviour, University of Cambridge, Cambridge, UK
Available online 7 February 2005.
What is a corvid? There are just over 120 species of corvids, a family of songbirds that includes the crows, ravens, rooks and jackdaws, as well as the more colourful jays, magpies and nutcrackers. Although belonging to the same order as nightingales and other birds with melodious songs (Oscines), corvids tend to be identified by their raucous calls. Little is known about corvid songs, perhaps because they are surprisingly quiet. Corvids can be found throughout the globe, except for the southern most tip of South America and the polar ice caps. In Britain, many of the common species, such as magpies and crows, steal other birds' eggs and raid agricultural crops. They are therefore treated with disdain by many birdwatchers and farmers.
Why study intelligence in crows? Corvids have not always had such a bad press. Native Americans believed that a raven had created the earth; the Norse god, Odin, consulted two ravens Hugin (Thought) and Munin (Memory) for their wisdom; and Aesop cast corvids as the smart protagonists in many of his fables. Along with their reputation in folklore as the wisest of animals, corvids have the largest brains for their body size of any bird. Perhaps most surprisingly, the crow brain is the same relative size as the chimpanzee brain. Other aspects of corvid biology also give us clues to their intelligence. In the wild, young corvids have an extensive developmental period before they become independent from their parents. This allows them more opportunities to learn the essential skills for later life. Many corvids also live in complex social groups. For example, in the cooperatively breeding Florida scrub-jay, several closely related family members share the responsibility of raising the young with the parents. Furthermore, rooks congregate in large colonies, where juveniles associate with many non-relatives as well as kin. In both cases, this long developmental period provides increased opportunities for learning from many different group members.
Perhaps it is not surprising then that many corvids are also renowned for their innovative feeding skills. For example, Japanese crows in Sendai City have learned to crack nuts safely by dropping them onto pedestrian crossings and waiting until the traffic lights turn red before retrieving the nut's contents. Rooks at a motorway service station in England have discovered a novel method for gaining access to food thrown in rubbish bins. Two birds cooperate in pulling up the bin liner and then either feeding from the raised food or tossing the contents onto the ground where the waiting crowd of colony mates reap the rewards.
As the crow flies… Most of the corvids that have been studied in detail hide food for the future in times of food abundance and then rely on memory to recover the food caches at a later date when food is scarce. For example, the Clark's nutcracker is estimated to hide over 30,000 pinyon seeds in many different places during the autumn in preparation for the harsh months ahead. Laboratory experiments have shown that they have highly accurate spatial memories, which enable them to recover these caches up to 9 months later. This is no mean feat when there are so many caches to keep track of, scattered throughout the territory, and when many aspects of the landscape change so dramatically across seasons. It has been suggested that Clark's nutcrackers rely on remembering the location of large vertical landmarks such as trees and rocks in the environment, because these landmarks are unlikely to be blown away or buried under the snow.
What do scrub-jays recall about past caching events? Although western scrub-jays do not hide as many seed caches as the nutcrackers, they are known to cache a variety of perishable foods, such as insects and fruit, as well as non-perishable nuts and seeds. In the laboratory, these birds demonstrate remarkable memories for what they have cached on a given day, and how long ago, as well as where they hid the various food items during that particular caching episode. This ability to remember the ‘what, where and when’ of specific past events is thought to be akin to human episodic memory, because it involves recalling a particular episode that has happened in the past. Until recently, this ability was thought to be unique to humans.
Avian espionage… Food-caching is a risky strategy, however, because the caches can be stolen by other birds. In addition to hiding their own food caches, corvids also play the role of thief: they watch and remember where other birds have hidden their caches and use this information to steal those caches when the owner has left the scene. When playing the role of thief, speed is of the essence and may make the difference between a successful raid and vicious attack by the owner of the food-cache. Not surprisingly, corvids also employ a number of counter strategies to reduce the risk that their own caches will be stolen by another bird. For example, they attempt to cache out of sight from potential thieves, or wait until the raider is distracted before hiding their caches, and if that is not possible, they hide caches in places that are difficult for the thief to see. When there is little option but to cache when others are around, then the birds will return to the caches once the others have left, and quickly re-hide any remaining caches in new places unbeknown to the potential raider.
Laboratory experiments have established that western scrub-jays use all these techniques to protect their caches from potential thieves, and only do so if another bird is present at the time of caching. Furthermore, they only move their caches to new hiding places if they have been thieves themselves in the past. Naı̈ve jays, even ones who have watched other birds caching but have never had the opportunity to raid those caches, do not do so. This suggests that experienced birds relate information about their previous experience of being a thief to the possibility of future theft by another bird, and adjust their caching behaviour accordingly. Using your own experience to predict another individual's future behaviour in relation to your own – ‘putting yourself in someone else's shoes' – is thought to be one of the hallmarks of Theory of Mind, another ability that was thought to be uniquely human.
Cultural tool use in crows? New Caledonian crows are extraordinarily skilled at making and using tools. In the wild, they make two types of tool. The hooked tools consist of twigs that are trimmed and sculpted into a functional hook, which the crows use to poke insect larvae out of tree holes. The crows also manufacture stepped-cut Pandanus leaves, which they use in different ways for different jobs: they make rapid back and forth movements for prey under soil, yet slow deliberate movements if the prey is in a hole. These tools are consistently made to a standardized pattern and carried around on foraging expeditions. The only other animals that display this diversity and flexibility in tool use and manufacture are the great apes. Thus, chimpanzees have been observed to manufacture a range of different tools that are used for specific purposes, and different geographical populations of chimpanzees use different tools for different uses, suggesting that there may be cultural variations in tool use. Observations of the crows' tool use in the wild also suggest similar levels of cultural complexity. For example, there is potential cumulative evolution in the complexity of stepped tools (increasing the number of steps required to make a more complex tool), analogous to minor technological innovations in humans. Crows from different geographical areas have different designs of tool, suggesting that crows may also show cultural variations in tool use.
Laboratory experiments confirm the sophisticated intellectual capabilities of these crows. One tool-using crow, called Betty, can manipulate novel man-made objects to solve a problem, such as reaching food in a bucket only accessible by using a hook to pull the bucket up. When the bent wire was stolen by another bird, Betty found a piece of straight wire that was lying on the floor, bent this wire into a hook and used it to lift up the bucket and reach the food! Betty proceeded to do this consistently. Furthermore, when given a tool box containing a variety of different tools to reach normally inaccessible food, she was able to select one of the correct length and width. So evidence of tool use and manufacture suggests that these crows can sometimes combine past experiences to produce novel solutions to problems.Feathered apes? Corvids are large-brained, social birds. They have an extensive developmental period in which they are dependent on their parents, and so have a long time-window in which to learn many different things from their parents and peers. They show a great propensity to find innovative solutions to novel problems, from the manufacture of tools to the protection of food from competitors. Furthermore, they appear to be particularly adept at predicting the future behaviour of conspecifics. These features are things they share in common with the apes. The common ancestor of mammals and birds lived over 280 million years ago, so it is hardly surprising that they have very different brains. It follows that intelligence in corvids and apes must have arisen independently in two groups with very different brains. Interestingly, the thinking part of the brain is correlated with propensity to innovate in both birds and primates, with the corvids and apes as the ‘star inventors’. So when it comes to intelligence, corvids are feathered apes.
Where can I find out more?
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“Reprinted from Current Biology, Vol 15 / Issue No 3, Author(s) Nicola Clayton and Nathan Emery, Corvid cognition, Page No. 1, Copyright 8 February 2005, with permission from Elsevier.”