Emery (2004) the Mentality of Crows

REVIEW The Mentality of Crows: Convergent Evolution of Intelligence in Corvids and Apes Nathan J. Emery1* and Nicola S. Clayton2 tools. Hook tools are crafted from twigs by Discussions of the evolution of intelligence have focused on monkeys and apes because trimming and sculpting until a functional of their close evolutionary relationship to humans. Other large-brained social animals, hook has been fashioned (13) and are used to such as corvids, also understand their physical and social worlds. Here we review recent poke out insect larvae from holes in trees studies of tool manufacture, mental time travel, and social cognition in corvids, and using slow deliberate movements (14). suggest that complex cognition depends on a ‘‘tool kit’’ consisting of causal reasoning, The crows also manufacture stepped-cut flexibility, imagination, and prospection. Because corvids and apes share these cognitive Pandanus leaves (14), which are used to tools, we argue that complex cognitive abilities evolved multiple times in distantly probe for prey under leaf detritus, using a related species with vastly different brain structures in order to solve similar series of rapid back-and-forth movements or socioecological problems. slow deliberate movements that spear the prey onto the sharpened end or the barbs n Aesop_s fable, a thirsty crow spied a Do Corvids Have the Brains for of the leaf, if the prey is located in a hole. pitcher containing a small amount of Complex Cognition? These tools are consistently made to a stan- I water. Unfortunately, the water was out The crow has a brain significantly larger dardized pattern and are carried around on of reach of the crow_s bill, but next to the than would be predicted for its body size (7), foraging expeditions (15). The manufacture pitcher was a pile of stones. The crow began and it is relatively the same size as the of stepped tools appears to be lateralized at placing the stones in the pitcher, thereby chimpanzee brain. The relative size of the the population level (16) and tool use at the raising the water until it could drink. Did the forebrain in corvids is significantly larger individual level (17, 18). crow understand that its actions would than in other birds (with the exception of Observations of the crows’ tool use in the increase the water level? some parrots) (2), particularly those areas wild suggest complex cognition. For exam- Throughout folklore, the corvids (crows, thought to be analogous to the mammalian ple, there is potential cumulative evolution in jays, ravens, and jackdaws) (Fig. 1) have prefrontal cortex: the nidopallium and meso- the complexity of stepped tools (increasing been credited with intelligence. Recent pallium (Fig. 2B) (8, 9). This enlargement of the number of steps required to make a more experiments investigating the cognitive abil- the ‘‘avian prefrontal cortex’’ may reflect an complex tool), which are analogous to minor ities of corvids have begun to reveal that this increase in primate-like intelligence in cor- technological innovations in humans (19). reputation has a factual basis. These studies vids (10, 11). There are also population differences in the have found that some corvids are not only types of tools manufactured (19), seemingly superior in intelligence to birds of other avian An Overview of Corvid Cognitive independent of ecological variability, which species (perhaps with the exception of some Psychology has been suggested as a form of culture in parrots), but also rival many nonhuman To fully appreciate how corvid and ape chimpanzees (20). primates. Traditionally, studies of complex psychology are similar, it is important to de- Laboratory experiments have confirmed cognition have focused on monkeys and apes scribe how corvids may represent their phys- the sophisticated cognitive abilities of these (1). However, there is no reason to assume ical and social worlds, and how these forms crows. One of them, Betty, appears to be that complex cognition is restricted only to of mental representation may be similar or capable of reasoning by analogy with her the primates (2). Indeed, the social intelli- dissimilar to those used by apes in solving previous experience with hooks, by modify- gence hypothesis (3) states that intelligence similar problems. We use the term ‘‘under- ing nonfunctional novel material (metal evolved not to solve physical problems, but standing’’ to convey the idea that corvids wire) into hook-like shapes to retrieve food to process and use social information, such as and apes reason about a domain (physical or in a bucket inside a vertical tube (21). Fur- who is allied with whom and who is related social) in a way that transcends basic asso- thermore, she chooses the correct length or to whom, and to use this information for ciative and reinforcement processes. diameter of tool out of a ‘‘tool box’’ con- deception (4). There is evidence that some Tool use and manufacture. Tool use is taining tools of different lengths and widths other large-brained social animals, such as defined as ‘‘the use of an external object as a to reach normally inaccessible food (22, 23). cetaceans, demonstrate similar levels of in- functional extension of mouth, beak, hand, Traveling mentally in time and space. telligence as primates (5). Corvids also or claw, in the attainment of an immediate Many corvids cache food for future consump- appear to meet many of the criteria for the goal’’ (12). Although many birds, primates, tion; either a large amount of seeds cached use of social knowledge in their interactions and other animals use tools, it is not clear over a wide area, which are stored seasonal- with conspecifics (6). whether any of these species appreciate how ly, or a smaller amount of higher-quality, tools work and the forces underlying their perishable material, which is recovered hours 1Sub-Department of Animal Behaviour, University of 2 function. Perhaps the most convincing can- or days later. These differences may require Cambridge, CB3 8AA, UK. Department of Experi- mental Psychology, University of Cambridge, CB2 didates are New Caledonian crows, who different cognitive abilities for successful 3EB, UK. display extraordinary skills in making and retrieval. Clark’s nutcrackers living at high *To whom correspondence should be addressed. using tools to acquire otherwise unobtainable elevations cache up to 30,000 pine seeds E-mail: [email protected] foods. In the wild, they make two types of over a wide area and can recover them up to www.sciencemag.org SCIENCE VOL 306 10 DECEMBER 2004 1903 R EVIEW 6 months later (24). By contrast, western scrub are cached, to learn their relative decay rates, and selectively searched for the nonperish- jays living in more temperate environments in order to recover food when it is still fresh able caches (27, 28). Furthermore, they could cache fewer of a wider variety of food items and edible. Laboratory studies have capital- recall when they cached different foods in the that differ in their level of perishability and ized on the fact that western scrub jays readily same location and could even distinguish are recovered after much shorter periods (25). cache perishable foods but will not consume between two caches of the same food type Cache recovery may require more than these items when they have degraded. that had been cached at different times (29). simply remembering where their caches are When jays were allowed to cache perish- These results suggest that scrub jays remem- hidden, for species that cache many types of able and nonperishable foods, they were able ber the ‘‘what, where, and when’’ of specific food. These species may need to process to remember not only which foods they caching events (episodic-like memory). This information about the location of the cache cached where, but also how long ago they representation of the time since caching is site, the type and perishability of the cached had cached them. If a short time had elapsed essential for the efficient recovery of perish- item, and the social context of caching (26). between caching and recovery, then they able food items (25, 26). When caching perishable food, it is prudent recovered the perishable food. But if they Social cognition of cache protection and to learn something about the decay rates of had cached a long time ago, they did not pilfering. Food storers should also be sensi- the food, and if two or more perishable foods attempt to recover the rotten degraded food tive to the social context of caching, because caches are susceptible to pilfering (30). For pilferers, the ability to quickly and efficient- ly locate caches made by others may be the difference between successful pilfering and attack by the storer. A number of corvids ob- serve conspecifics caching and demonstrate excellent observational spatial memory for the location of another bird’s caches (25, 31, 32). The use of observational spatial memory as a pilfering strategy may differ between species depending on level of sociality, and as such may be an adaptive specialization (33). Do social pinyon and Mexican jays, and territorial Clark’s nutcrackers, remember where another bird has cached (31, 34)? Pinyon jays remembered the specific location of others’ caches after 1 and 2 days, as did Mexican jays, whereas Clark’s nutcrackers were only as accurate as chance after 1 day. After 2 days, the Clark’s nutcrackers were only accurate at recovering their own caches, not those they had observed. (34). This find- ing supports the adaptive specialization of the social learning hypothesis in corvids; however, another study is more ambiguous (35). Furthermore, western scrub jays are semiterritorial, and they have highly accurate observational spatial memories (25). The social context of caching may be viewed as an arms race between storers and pilferers, in which storers use counterstrat- egies to minimize the risk of having their caches pilfered (36).

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