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The scheming minds of crows

20 June 2007 news service
Joanna Dally

IF THE working day of a western scrub-jay were ever subjected to a time-and-motion study, the results would not look very impressive. Like many birds and mammals, these members of the crow family put considerable time and effort into hiding food, which they recover later. That in itself is not the problem. It is the scrub-jay's habit of returning to a cache, digging it up and then hiding it again somewhere new that seems so inefficient.

Nicky Clayton first witnessed this strange behaviour on the campus of the University of California, Davis, where the birds would make a beeline for discarded remains of student picnics and then secrete the scraps in nearby shrubbery. When she noticed that individuals sometimes returned later to secretly rebury their spoils, she wondered why they would go to so much trouble.

Now professor of comparative cognition at the University of Cambridge, Clayton is well aware that crows and their ilk, known collectively as corvids, are among the most intelligent of all animals. As well as caching food, scrub-jays habitually steal hidden items from one another. She suspected that the re-hiding might be a way of foiling potential thieves. If so, she reasoned, studying it could be a good way of finding out what these birds understand about the perceptions and intentions of others. What Clayton and her colleagues - including myself - have since discovered has caused quite a stir because it challenges the received wisdom that complex social intelligence is unique to great apes.

The crow family extends far beyond the black-feathered urbanite crows, rooks and ravens that immediately spring to mind. In fact, it encompasses around 120 species - including the colourful jays, magpies and nutcrackers - and they are found in every environment except the polar ice caps. Their intelligence is well known and is often explained as an evolutionary adaptation to group living. Many species live in a complex social environment where it is necessary to track not only their own relationships but also those of the others in their group. They are notoriously playful, especially the young birds who have a long developmental period during which they learn from group members. Several species have even been observed making tools - a talent that was thought to be the preserve of primates (New Scientist, 17 August 2002). Corvids also display levels of flexibility to rival great apes when solving novel problems.

Clearly, corvids are no birdbrains, yet getting an insight into the mental life of an animal so different from humans is not easy. Studying the food-hiding and stealing habits of scrub-jays and other corvids was the perfect opportunity to do just that.

In 2001, Clayton, working with colleague and husband Nathan Emery, carried out the first of many studies of the tactics scrub-jays use to protect their hoards. They allowed jays to hide worms either while they were alone or when another bird was watching, and to recover the hidden items in private later that day. Worms are the "Belgian truffles" of the jay's gastronomic world, so the researchers anticipated that birds would make every effort to protect their stores. They found that when jays were allowed to return to their stash, those that had hidden worms under the gaze of a would-be thief moved them to new sites. Birds did not move worms they had hidden in private, however. "By selectively re-hiding those items others witnessed being cached, scrub-jays prevent their competitor using memory to relocate and steal their hoards," says Emery (Nature, vol 414, p 443).

Clayton's suspicion was correct - re-hiding appears to be a strategy to limit the chances of being burgled - and it is not the only trick jays use to outwit potential thieves. In a study I carried out with Clayton and Emery, we found that when hiding worms with another bird around, jays prefer to cache their meal behind a barrier that blocks their rival's view (Animal Behaviour, vol 70, p 1251). That might not sound very clever, but it suggests they may be able to see things from the visual perspective of another individual. In other words, they might understand that another bird learns about the world through its sense of vision. This is an insight into the mind of another that has traditionally been thought the preserve of great apes. There is an alternative explanation, however. Jays' preference for hiding food outside the field of view of a potential thief might simply reflect the old adage that out of sight is out of mind.

An encounter between jays and a camera crew provided the inspiration to test these two possibilities. "Whilst a film crew was recording jays, we noticed that storing birds were heading for the shadows cast by the sound man's boom," says Clayton. "Perhaps jays use shade to their advantage. Hiding food in the dark corners might make it harder to be seen by potential thieves - from local jays to foreign cameramen."

Translating this idea to the lab, we gave jays the option of hiding nuts in well-lit or shady sites. When no rival was watching, they showed no preference between the two, but when watched by a potential thief, the jays shunned bright sites, preferring to hide their nuts in the shadows. The potential thieves were always in view, so never "out of mind", suggesting that the decision to cache nuts in hard-to-see places does arise from an understanding of the visual perspective of others (Biology Letters, vol 271, p S387).

Given the level of subterfuge inherent in corvid feeding behaviour, you might expect the social life of these birds to be mired in suspicion and mistrust. You would be wrong. Members of the crow family are famed for their fidelity, often mating for life. Recognising your partner and maintaining that relationship is an important ability for a social animal. For jays this extends to caching: mated pairs are less likely to re-hide items that they have hidden while their partner was present, and even go so far as to chase would-be thieves away from the stores of their spouse.

This got us wondering to what extent these birds can keep track of the competition. Remembering which other birds have witnessed particular items being hidden would increase a storer's ability to protect its stash. To look at whether jays are capable of this mental feat, Clayton, Emery and I conducted another experiment in which jays hid food in two successive sessions, each in the presence of a different observer. Later that day, the hiders were allowed to return to their caches in the presence of one of the two observers. We discovered that jays tended to re-hide items if watched by the same bird that had seen them hiding the stash the first time, moving caches repeatedly as if to confuse the observer. But they did not disclose the location of items hidden in the presence of the other bird by moving them.

The discovery that jays can remember who was present when they hid a cache was particularly intriguing because it suggests they can discriminate between individuals with different knowledge states. However, as we pointed out when we published the study, this does not necessarily require human-like memory. Instead, the birds could be acting on the basis of behavioural predispositions and learned conditional discriminations. In other words, they might have an innate tendency to re-cache items that they were observed hiding which, combined with an ability to discriminate between individuals that were present or absent from a particular hiding session, would result in the observed behaviour (Science, vol 312, 1662).

Our studies have revealed much about the intelligence of caching jays, but the reason hiding behaviour is so intriguing is that it involves social interaction between two birds - the hider and the thief. Thomas Bugnyar from the University of St Andrews, UK, and Kurt Kotrschal from the Konrad Lorenz Research Station, in Gr'nau, Austria, who study caching in ravens, liken it to a "cognitive arms race". In these games of hide-and-steal, each bird has a dual role. "Every player not only needs to develop strategies to prevent other birds burgling their own caches but also must gather information on others' caches, perhaps through spying," Bugnyar says.

Like us, Bugnyar sees striking parallels between the human world of espionage and that of feathered thieves. Just as secret service agents engage in covert surveillance, raven pilferers keep their distance when spying on caching birds, Bugnyar and Kotrschal have observed. Watching from the edge of trees and rocks, these stealthy competitors generally wait for cachers to leave the scene before plundering their hoards.

Ravens also have strategies for outwitting their superiors. Stealing a dominant bird's cache is a risky business: if caught in the act, a subordinate raider would undoubtedly suffer a physical rebuke. That doesn't mean lower-ranking birds refrain from stealing, but they do their best to avoid an aggressive backlash. Instead of heading straight for hidden caches, raiders poke around in places that do not contain any food. "By distracting the cache owner, stealers stand a better chance of getting away with theft," says Bugnyar. One interpretation of this behaviour is that subordinate ravens are trying to trick dominant birds into thinking that they do not know where the food is - which would be very clever. "What we don't yet know is whether thieving ravens are attempting to manipulate what the storer believes, rather than how they will behave," Bugnyar admits.

Nevertheless, the fact that both hiders and thieves can implement a wide variety of strategies flexibly, depending on the presence or absence of specific individuals, does indicate that they constitute more than simple hard-wired responses. So how do corvids acquire this suite of behaviours?

In trying to answer this question, Clayton and Emery have made the exciting discovery that not all individuals re-hide food. While experienced thieves engage in high levels of re-caching after being observed hiding food, birds that had never stolen another bird's cache move few, if any, items. It would appear that it takes a thief to know a thief. This suggests that scrub-jays use their past experiences of, say, having been a thief, to predict what another individual, in this case the potential pilferer, might do. "Experience projection has yet to be demonstrated in any of the great apes other than humans," says Clayton. "Most people have assumed that it was a uniquely human trait, but the jay studies challenge this assumption."

"Birds that have never stolen do not re-hide their cache. It takes a thief to know a thief"

The possibility that scrub-jays appear able to simulate another's viewpoint is ruffling some feathers. If corvids can understand each other in ways that were once thought exclusive to great apes, then this challenges our assumptions about the evolution of social intelligence. Our common ancestor with these birds lived over 300 million years ago, so the capacity for social intelligence would have had to evolve independently at least twice. This evolutionary convergence in intelligence is all the more exciting given the divergent structures of the mammalian and avian brain (see "Who's a clever bird?").

We don't know the extent to which social competition was responsible for shaping the advanced cognitive abilities of corvids. It is generally accepted, however, that so-called Machiavellian intelligence has been an important factor in the evolution of our own big brains. Recognising the parallels between apes and crows might give new insights into the evolution of both. "Corvids and apes are so similar in many aspects of behaviour and cognition that crows could be considered feathered apes," says Emery.

Joanna Dally is in the sub-department of animal behaviour at the University of Cambridge

From issue 2609 of New Scientist magazine, 20 June 2007, page 34-37 mg19426091.700;jsessionid=FFIOPNFLLJDF

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