Tool-related cognition in New Caledonian crows.


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Tool-related cognition in New Caledonian crows.

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Tool-related cognition in New Caledonian crows.
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Comparative Cognition & Behavior Reviews
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Bluff, Lucas A.
Weir, Alex A. S.
Rutz, Christian
Wimpenny, Joanna H.
Kacelnik, Alex
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New Caledonian Crows ( local )
Physical ( local )
Cognitive ( local )
Tool-Related Behaviour ( local )
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The extent to which non-humans understand their physical world is controversial, due to conceptual and empirical difficulties. We examine the evidence for physical understanding in the remarkable tool-oriented behaviour of New Caledonian crows, which make several types of tool in the wild and show prolific tool-related behaviour in captivity. We summarize our own research into the cognitive processes involved in tool behaviour in this species, and review comparable studies in other birds and primates. Our main laboratory findings are: tool-related behaviour emerges in juvenile crows that had no opportunity to learn from others; adult crows can make or select tools of the appropriate length or diameter for tasks; and one crow, at least, can bend and unbend novel material to match task requirements. Although these observations are striking, they do not prove that this species is capable of understanding physical causality, as one cannot exclude explanations based on inherited proclivities, associative learning, and generalisation. Despite this, we argue that the conventional mechanisms become less likely as such observations accumulate. We conclude that while no adequate, non-verbal test for understanding exists, continued work with New Caledonian crows will help us to ask the right questions.
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Comparative Cognition & Behavior Reviews, Vol. 2, no. 1 (2007).

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Tool-related Cognition 1 Tool-related Cognition in New Caledonian Crows Lucas A. Bluff, Alex A. S. Weir, Christian Rutz, Joanna H. Wimpenny, and Alex Kacelnik University of Oxford ties. We examine the evidence for physical understanding in the remarkable tool-oriented behaviour of New Caledonian our own research into the cognitive processes involved in tool behaviour in this species, and review comparable studies in opportunity to learn from others; adult crows can make or select tools of the appropriate length or diameter for tasks; and one crow, at least, can bend and unbend novel material to match task requirements. Although these observations are striking, they do not prove that this species is capable of understanding physical causality, as one cannot exclude explanations based on inherited proclivities, associative learning, and generalisation. Despite this, we argue that the conventional mechanisms become less likely as such observations accumulate. We conclude that while no adequate, non-verbal test for understanding exists, continued work with New Caledonian crows will help us to ask the right questions. Our group has studied tool-oriented behaviour (TOB) in New Caledonian crows ( Corvus moneduloides ) for the documentation of wild New Caledonian crow behaviour by Gavin Hunt and associates from Auckland University (Hunt, 1996, 2000a; Hunt, Corballis, & Gray, 2001; Hunt & Gray, 2003). Here we present a progress report that focuses on ex perimental studies with captive crows in Oxford. We discuss data collected by our New Zealand-based colleagues and to theoretical issues faced by other researchers in comparative cognition. We address—but do not solve—the epistemologi physical understanding and reasoning in non-human species. Our broad perspective is that while tool-related behaviour is not necessarily associated with unusually sophisticated cog nition, it is likely to be unusually revealing about the cog nitive processes and the level of understanding involved in Volume 2, pp 1-25 2007 Figure 1. A New Caledonian crow uses a stick tool to ex tract mealworms from a drilled log in the Oxford laboratory. Photo: Lucas Bluff (reprinted with permission). Lucas A. Bluff, Alex A. S. Weir, Christian Rutz, Joanna H. Wimpenny, and Alex Kacelnik, Department of Zoology, Uni versity of Oxford, Oxford, UK. We thank Gavin Hunt and Russell Gray for useful discussion over the years. This work was supported by the BBSRC (grant BB/C5 1 7392/ 1 to Alex Kacelnik), the University of Oxford, a fellowships (Brasenose College to Alex A. S. Weir; Linacre College to Christian Rutz), and a BBSRC studentship (to Jo anna H. Wimpenny). We gratefully acknowledge the valuable contributions made by Sara Shettleworth, Nathan Emery, and Russell Gray in refereeing this article. Correspondence concerning this article should be addressed to Alex Kacelnik, Department of Zoology, University of Ox kacelnik@zoo.ox.ac.uk

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Tool-related Cognition 2 Although TOB is not necessarily associated with unusual cognition, the making and using of tools may be especially revealing from a cognitive perspective. Making and using a valuable glimpse of an organism’s use of abstraction or generalisation in the physical domain. Tool use entails a be havioural richness that can be exploited in controlled experi task by deployment of a previously reinforced behaviour or a combination of such behaviours. It is challenging to design Uniquely amongst non-mammals, New Caledonian crows make and use a number of distinct tool types in the wild and in captivity (Figure 2), some of which involve considerable processing of the raw materials (Hunt, 1996; Hunt & Gray, 2004a, 2004b). Tool use and manufacture by animals has at tracted considerable interest from scientists and the general public, probably because of its rarity and its apparent as sociation with the human lineage. Whilst it is now widely accepted that tool use per se is not indicative of unusual in telligence (e.g., Alcock, 1972; Beck, 1980, 1986; Hall, 1963; Hansell, 1987), the remarkable complexity of New Caledo nian crows’ natural TOB has often led observers (lay people as well as scholars) to assume that this species may possess exceptionally advanced cognitive abilities. However, such best, as the motor complexity of a behaviour offers no guide amples of complex architecture—typically in the form of nests—throughout the animal kingdom (Hansell, 2005), none of which are thought to require generally elevated cog nitive abilities. Natural behaviour arises through the interaction of the ge netic endowment with a number of ontogenetic processes that include trial-and-error, associative and social learning, and possibly reasoning. It is axiomatic that the contribu processes such as reasoning or insight, cannot be reliably inferred from observing spontaneous behaviour of wild animals without experimental investigation. Even when elusive because virtually everything an adult animal does is affected by previous associative learning and generalisation. behaviourists’ reluctance to even invoke the possibility of entities such as reasoning or understanding, and we do have sympathy with this argument by parsimony. However, the complete learning history of anything but newborn individu als is never fully known. Therefore, although attributing in novative problem-solving to a hypothetical combination of reinforced learning and generalisation appears parsimonious as speculative as accounts involving abstract forms of infor derstanding’. We are fully aware that such information-processing mechanisms are not alternatives to associative learning but may act in concert to produce innovative behaviour. How ever, it would seem agreeable to most that, when observing a behavioural innovation, the more contrived the required generalisation from previously reinforced behaviour, the more plausible it is to invoke the existence of alternative mechanisms involving higher level concepts (we have made similar points elsewhere; see Weir & Kacelnik, 2006). This is the theoretical framework in which we seek to explore the folk-psychological labels, such as reasoning, understanding, and creativity, in tool-oriented behaviour of our model spe cies. Figure 2. New Caledonian crows make and use a range of tool types. The tools shown here were made from: (a) twigs; (b) Pandanus leaves; (c) leaf stems and cardboard; and (d) moulted crow feathers. The Pandanus leaf tools and coun terparts were collected by Gavin Hunt in New Caledonia, the rest were made in captivity in Oxford. From Figure 26.1, page 518, “Cognitive Adaptations for Tool-related Behav iour in New Caledonian Crows,” by A. Kacelnik, J. Chap pell, A. A. S. Weir, and B. Kenward. In Comparative Cogni tion: Experimental Explorations of Animal Intelligence (eds. Wasserman, E.A., & Zentall, T.R.), pp. 515-528. Copyright 2006 by Oxford University Press. Adapted with permission.

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Tool-related Cognition 3 and interpret such experiments, but TOB offers a context in which the opportunity for innovation is greater than in rewards using binary manipulanda such as pecking keys or levers. So far, we have investigated two different aspects of New to the development of fully-functional TOB, and the cogni tive processes that are involved in the deployment of TOB in adult crows. While both levels of enquiry are necessary to understand this species’ cognitive capacities, it is impor tant to recognise that, at different periods within a crow’s life, different mechanisms may govern the expression of functional tool use. For example, observing the spontaneous emergence of a non-reinforced behaviour during early devel opment leads us to infer the presence of a genetic propensity for that behaviour, but this does not imply that its subsequent deployment is unaccompanied by information-processing mechanisms that would qualify as higher cognition. Indeed, genetic predispositions are thought to be the building blocks through which human children learn about the properties of vise solutions to novel problems through processes such as reasoning. We acknowledge that exploring the cognition behind ac tion, especially in the context of physical understanding, they believe that they are not hampered in reaching a rel evant, currently active goal by lack of knowledge about that based on goals and knowledge to non-humans is not easy. Most research to date into the causal understanding of nonbehaviour is generated by associative versus inferential (or reasoning) processes (e.g., Call, 2004; Dickinson, 2001), (an event or action) is equated with the ability to infer the causal agent. However, this debate has been hampered by a the advocates for such processes tend to formulate their ar guments verbally, rather than mathematically, which makes them almost impossible to refute. Some authors do explicitly sitional knowledge in a controlled (i.e., slow, effortful, con scious, and/or intentional) manner” (de Houwer, Beckers, & Vandorpe, 2005, p. 240). However, most researchers (includ ing, at times, ourselves in previous publications) informally invoke reasoning or other cognitive processes for situations the mathematical properties of associative learning and what behaviours it can and cannot explain (e.g., Dickinson, 2001) and whether other algorithms such as causal Bayes nets pro vide a better explanation (e.g., Blaisdell, Sawa, Leising, & Waldmann, 2006). We feel that this debate does not address animals capable of understanding and reasoning about cau sality in a qualitatively similar way to humans? Penn and Povinelli point out that human causal knowl allocentric, coherent, abstract explanations for the unobserv able causal mechanisms that govern a given domain,” and can be generalized freely to disparate concrete examples that share little to no perceptually based featural similarity” (Penn & Povinelli, 2007, p.107). Mechanisms such as associative learning are undoubtedly involved in the process of form ing these theories, but the key point is that behaviour should The main goal in our laboratory work with New Cale knowledge underlies their TOB—or in other words, whether they understand how their tools work. In spite of all the ca veats listed above, we still feel that it is helpful to distinguish between behaviour shaped by known or easily conceived ex periences of reinforcement (i.e., trial-and-error learning) and behaviour which appears to result from an abstract process of inference. It is worth noting that the methods typically used to in vestigate cognition in non-verbal animals are fundamentally different from those employed in studies with humans. To probe adult humans’ understanding of the physics underly ing their use of a tool, one can ask them to verbalise their reasoning. This does not prove that their actions are guided by their expressed beliefs (which could be true or false re that they understand why or how the tool works (Overskeid, 2005). Regardless of whether the use of the tool is competent, tions is correct, one can infer something about the existence and quality of understanding (a narrative based on a super stitious belief such as the gamblers’ fallacy is a mistaken but interesting form of understanding). Even this limited level of enquiry is impossible with non-human animals, so we have to rely on observing and interpreting tool-using performance

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Tool-related Cognition 4 true beliefs. We are condemned to being over-conservative and denying any understanding to an animal that does have a theory and guides its behaviour by it, if this theory happens to be wrong. Our general experimental approach is to present our sub ations that members of the species are inclined to tackle, are as novel (namely as different from previous experiences in which reinforcement for behavioural components have oc curred) as possible (similar to the approach taken by Hauser, sessed abstract, theory-like explanations for how and why their tools operate, we could expect that in most such ex not be immediately successful. Each single experiment, therefore, provides limited information regarding how much of the observed behaviour is strictly novel, the outcome of reasoning, or both, particularly since (a) no task in which the birds willingly participate can ever be absolutely novel, previous experience. This means that, even though we trans form the tasks as radically as possible from one experiment to another, there is no discrete threshold separating solutions produced by pure reinforcement of random behaviour from those resulting from understanding or reasoning. used intuitively in every-day language to denote high-level cognition, let alone to investigate them empirically in ani mals. Reasoning, understanding, and logical inference are neither the opposite of genetically-channelled actions (which do not require reinforcement), nor of associatively learnt ac tions (which do). While parsimony advises against invoking these very opaque processes when more transparent ones are available, we still believe that the richer the number of more useful it is to invoke them. The main part of this review consists of two broad sec tions distinguishing the development and deployment of TOB. For some of our most cherished questions, such as the extent to which New Caledonian crows can use reasoning to solve physical problems, or what ecological and evolution ary circumstances led to the unusual behaviour of this spe cies, we can only offer informed speculation. However, we do hope to show that some parts of the puzzle are being un ravelled and that there is good reason to be optimistic about future progress, provided we advance with caution and are able to proceed simultaneously with experimental and ob servational research. Tool-oriented Behaviour in the Wild The archipelago of New Caledonia is situated some 1,500 km east of the Australian mainland. New Caledonian crows are endemic to the main island of Grande Terre and one of its sister islands, Mar, where they were introduced by humans (ca. 1850s; Dlacour, 1966). Crow tool use is featured in New Caledonian folklore and early European accounts, and stick tool use was reported by Orenstein in 1972. However, it was not until 1996 that the complexity and diversity of New Caledonian crow TOB was described by Gavin Hunt (Hunt, 1996). While many species use tools (Beck, 1980), the habitual use of multiple types of tool in the wild was thought to be restricted to primates (e.g., Parker & Gibson, 1977). Hunt and colleagues have demonstrated that, as a species, wild crows use a variety of tools, which they classi Figure 3. of Pandanus trees (top). Crows produce tools from leaf edg es, leaving distinct ‘counterparts’ behind (bottom). These ished tool (see Figure 2b). Photos: Christian Rutz (reprinted with permission).

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Tool-related Cognition 5 of individuals, the intriguing possibility of cultural transmis sion remains an untested hypothesis (see Laland & Janik, that it is not yet possible to compare variation in tool shapes produced by individuals from different populations, which requires the observation of large samples of individuallyVery little is currently known about the behavioural and social ecology of these crows in the wild, other than that their parents for relatively long periods, and that they are found in dry and humid forest habitats in New Caledonia and in savannah and agricultural areas (reviewed in Kenward, Rutz, Weir, Chappell, & Kacelnik, 2004). Field studies with marked individuals by both research groups are underway (Figures 4 and 5), but until further reports are available there is hardly any basis for speculation about the reasons for their unique tool-related specialisation. 2000b; Hunt & Gray, 2002; Rutledge & Hunt, 2004), hooked twigs or vines (Hunt, 1996; Hunt & Gray, 2004a), and tools torn from the leaves of the Pandanus tree (Figure 3; Hunt, 1996, 2000a; Hunt et al., 2001; Hunt, Corballis, & Gray, 2006; Hunt & Gray, 2003, 2004b). Like some other corvids (Cristol & Switzer, 1999), New Caledonian crows drop nuts to break them open (Layard & Layard, 1882), but using an unusual technique they wedge the nuts in tree forks before rolling them off (Hunt, Sakuma, & Shibata, 2002), perhaps The shape of tools the crows produce from Pandanus leaves varies across New Caledonia, leading to the sug gestion that tool-manufacturing skills may be transmitted and maintained culturally, perhaps even with a human-like ratchet effect where innovations are accumulated over time (Hunt, 2000a; Hunt & Gray, 2003). Since these data are ob servational, rather than experimental, and are based on the collection of tool counterparts made by an unknown number Figure 5. Wood-boring beetle larvae (Cerambycidae; top) live in dead Bancoulier trees. New Caledonian crows use stick tools to probe into their burrows and extract the larvae; sometimes tools can be found still inserted into holes (bot tom). Photos: Lucas Bluff and Christian Rutz (reprinted with permission). Figure 4. New Caledonian crows are found across the main island in a range of habitat types. The images show two of our present study sites in dry (top; note base camp at centre of image) and humid forest (bottom). Photos: Lucas Bluff and Christian Rutz (reprinted with permission).

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Tool-related Cognition 6 Development of Tool-oriented Behaviour nian crow, it is hard even for seasoned behavioural scientists to avoid interpreting the behaviour in terms of planning and sions that highlights the importance of a program of research into the evolutionary, ecological, ontogenetic, and cognitive underpinnings of what the crows do. All classical ethologi cal questions, from causation and development to function and phylogenetic history, are pertinent and hard to answer. Various hypotheses about causation and concomitantly about the reasons why similar behaviour is not observed in other avian species can be used to frame the problem. The set of genetically determined rules, in the sense applied to most animal architecture (e.g., nests, spiders’ webs; Hansell, 1984, 2005); (b) TOB may develop because of particularly how to solve problems using tools—an inherited capacity for rational insight or a habitat offering special opportunities veniles may have an inherited tendency to manipulate physi tool use by their own history of reinforcement—in this case, use) would be the relevant inherited trait characterising the species; or (d) the behaviour may be passed on through imi tation of other tool-using individuals. Hypothesis (d) ignores the problem of how TOB was acquired by the population in specialisation in itself, but a consequence of an enhanced general tendency for social learning. These hypotheses are not mutually exclusive, and it is reasonable to expect that a grain of truth may be associated with each of them and also with other possibilities. One way to eliminate some, however, is to monitor the development of spontaneous development of behaviour sets boundaries to the need to invoke learning or social transmission and also serves to establish to what extent TOB is an evolved adaptation in this species. Distinguishing between reason pect a gradual emergence of tool use under hypothesis (c), emergence of successful tool use, whereas reasoning should lead to a sudden acquisition of successful behaviour, with a In the summer of 2004, we reared four crows in our Ox ford laboratory (Kenward, Rutz, Weir, & Kacelnik, 2006; Kenward, Weir, Rutz, & Kacelnik, 2005). Three individuals removed from the nest one day after hatching. We investi tool use, and Pandanus tool manufacture. Development of Tool Use To make the best use of our limited sample size, we de ronments. From the time they started to venture outside their use (but not of tool making), in which a human foster parent extracted food from holes and crevices (Figure 6). The other but otherwise received the same degree of overall contact with their human caretakers and, importantly, were fed near holes to control for the possible effect of local enhancement. One of these untutored birds (Corbeau) never saw any toolhave observed a few accidental instances of a keeper pick them in any purposeful way). Figure 6. A captive-bred juvenile crow watches a human tutor demonstrating tool use. Photos: Charlotte Burn (re printed with permission).

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Tool-related Cognition 7 from crevices with stick tools (Figure 7; Movie 1), with no obvious difference in the onset of tool using between in dividuals from different treatment groups (Kenward et al., systematic comparisons are still lacking, other corvids such as magpies ( Pica pica Aphelocoma californica Garrulus glandarius daws ( Corvus monedula ), rooks ( C. frugilegus ), common ravens ( C. corax ( C. brachyrhynchos, C. corone, C. macrorhynchos ) are of none shows a tendency to develop tool use spontaneously. Anecdotal episodes of tool use in wild and captive corvids have been reported (Andersson, 1989; Boswall, 1978, 1983; Caffrey, 2000; Cole, 2004; Gayou, 1982; Jones & Kamil, 1973; Reid, 1982), but all of these are examples of unusu al, idiosyncratic behaviour in one or a few individuals (for example, one American crow observed by Caffrey (2000) broke off and used a tapered piece of wood as a tool, of a similar shape to the stepped-cut Pandanus tools made by New Caledonian crows). The time-course and nature of tooluse development was strikingly similar between all of our In this regard, the crows appear to be similar to other birds Cactospiza pallida; Tebbich, Taborsky, Fessl, & Blomqvist, 2001), the only other bird species that habitually uses stick tools in the wild; in Egyptian vultures ( Neophron percnopterus ; Thouless, Fanshawe, & Bertram, 1989), which use stones to crack open ostrich eggs; and in hyacinth macaws ( Anodorhynchus hyacinthinus; Borsari & Ottoni, 2005), which use slivers of wood or leaves as wedges while cracking nuts. Food retrieval in all hand-reared New Caledonian crows contained components of the functional, mature behaviour branching), where the bird holds a twig in its beak and moves its head back-and-forth in a manner that would be ap propriate for probing a hole or crevice to extract food; in this case, however, the twig is moved whilst touching against the surface of another substrate (such as a perch), rather than be ing inserted into a concavity. Precursor behaviours have also been reported for the development of tool use in the wood snail-smashing in song thrushes ( Turdus philomelos ; Henty, 1986), caching in Parids (Clayton, 1992), and nest-building in village weaverbirds ( Textor cucullatus ; Collias & Collias, 1964). The presence of precursor behaviours in all our handreared crows begs the question of whether they play a role in enabling the developing crow to learn about the conse action’ development is believed to be central to the devel opment of tool-oriented behaviours in the human child and Figure 7. Hand-reared juveniles started probing into holes same age, regardless of whether they had been tutored or not. Top: from Figure 1 (a) (photo: Lucas Bluff), page 1331, “Development of Tool Use in New Caledonian Crows: Inher Rutz, A. A. S. Weir, and A. Kacelnik, Animal Behaviour, 72, 1329-1343. Copyright 2006 by The Association for the Study of Animal Behaviour. Adapted with permission. Bottom: from Figure 1a (photo: Ron Toft), page 121, “Tool Manufacture by Naive Juvenile Crows,” by B. Kenward, A. A. S. Weir, C. Rutz, and A. Kacelnik, Nature, 433, 121. Copyright 2005 by Nature Publishing Group. Adapted with permission.

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Tool-related Cognition 8 other primates (Gibson & Pick, 2000; Lockman, 2000). The crows’ precursor behaviours did not result in (and hence were not shaped by) reinforcement through food acquisition—all precursor actions were performed weeks before successful food retrieval was observed. This eliminates the possibility that tool use develops as the result of an increased tendency for purely random emphasises the role of inherited traits together with some tool use (for further discussion, see Kenward et al., 2006). The development of tool use without social input, the exis (namely stereotyped tool-related actions that emerge without reinforcement), and the fact that New Caledonian crows fre quently use tools in the wild, indicates that tool use has been or was in the past, an adaptive specialisation. In chimpanzees ( Pan troglodytes ) and capuchins mon keys ( Cebus apella and individual learning precedes functional tool use, with a notable increase in behavioural complexity during develop & Adams-Curtis, 1997; Lonsdorf, 2005). Furthermore, these species seem to have a predisposition for certain ac Cebus apella Pan troglodytes TOB in crows (Kenward et al., 2006) is similar to that of capuchin monkeys (Fragaszy & Adams-Curtis, 1997) in that non-functional (precursor) behaviours persist until after suc cessful tool use has developed. As a conceptual model, the ontogeny of TOB seems to follow a similar path to the devel Members of the species are endowed with a host of genetic predispositions to acquire the behaviour, but learning—and social learn ing—determines the fate of these predispositions (Marler & Slabbekoorn, 2004). It is thus necessary to consider to what extent social factors can affect the development of TOB in New Caledonian crows. While the onset of tool use did not differ between birds development did. Compared to the untutored birds, the two lated to tool use, such as twig carrying and inserting, but did not differ in measures of general motor development, such as locomotion and carrying of non-food, non-twig items (Kenward et al., 2006). The sensitivity of crows to social factors was further highlighted by the results of a simple been manipulated by the tutor. Both birds had a strong pref by the human experimenter. In the wild, such stimulus, lo cal enhancement, or both may play an important role in the acquisition of certain aspects of TOB, such as the choice of appropriate raw materials for tool manufacture. In primates, notably chimpanzees, there is no doubt that social learning ented behaviours (e.g., Lonsdorf, 2005, 2006). On the other 2001). Development of Pandanus Tool Manufacture When crows tear a tool out of a Pandanus leaf, a distinc ing to island-wide surveys by Gavin Hunt and colleagues, Pandanus tools conform to three distinct types—narrow, wide, or stepped—and the relative frequencies of these types vary across New Caledonia without any obvious asso ciation with relevant environmental factors (Hunt, Corballis, et al., 2006; Hunt & Gray, 2003). This observation consti tutes the basis for the suggestion of a cumulative form of cultural transmission of tool technology. Our experimental results show that New Caledonian crows pay attention to the behaviour of others, which is a prerequisite of the culture hypothesis. However, other important pieces of the puzzle manufacture Pandanus tools, and if they do, whether they can produce the different tool shapes observed in the wild. The greater the degree of competence shown by untutored animals, the less we need to invoke social determinants. Pandanus leaves when they were between 3 and 4 months old (the two tutored birds were exposed to Pandanus around 2 months old, but were too young to tear at the leaves). To do so, we mounted individual Pandanus their behaviour (no birds received demonstrations). All four bird (Corbeau) manufactured and used a functional tool on have been used as tools, although only Corbeau was actually observed extracting food with them. received demonstrations of tool use (Uek and Nalik) were now allowed to observe a human making tools from leaves

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Tool-related Cognition 9 and using these to retrieve food (but not to keep them or use was given four human-made tools plus intact Pandanus leaves (mounted more naturalistically than previously, on an received two due to a shortage of available leaves. Func produce non-functional strips (Kenward, 2006). This is con captive-born New Caledonian crows will tear tool-shaped strips from Pandanus leaves in the absence of social inputs, and hence without a requirement for culture. However, the pieces removed from the leaves and used as tools were crude in shape and manufactured using a different technique from that used by (at least) one wild crow observed by Hunt and Gray (2004b). Therefore, the possibility remains that social Pandanus tool manufacture in wild crows. occurred for several reasons, some of which are supportive of the culture hypothesis while others argue against it. Rea sons why invoking culture may not be necessary include the 1. Environmental limitations. The lab experiments may underestimate the tool-making ability of untutored birds. Reasons for this may be that the leaves available to the crows in Oxford were not from the same (sub)species of Pandanus that is typically used by wild crows in New Caledonia, and differences in leaf morphology may well as part of a natural tree, and the mode of accessing the food ad libitum , so a lack of nutritional need and a sur 2. Developmental limitations. The birds were still young, been given access to raw materials too late during their and opportunity to practice. We only had a limited sup ply of fresh Pandanus leaves and only offered them on a handful of occasions. 3. Individual differences. It is possible that only some indi Pandanus tool manufacturers, and our small sample may not have included any such birds (the level of individual specialisation in the wild is not yet known). 4. Genetic differences. Pandanus -tool manufacture may knowledge) none of our wild-caught captive crows come from areas of New Caledonia where Pandanus tools are made (see Kenward et al., 2004, for details of capture genetic adaptations. In support of the culture hypothesis, it could be that, while some aspects of TOB are narrowly canalised genetically, so manufacturing techniques, tool designs, or both. These op tions are clearly separable with further data, and forthcom ing research will clarify the issue. Social learning need not involve faithful imitation of the exact motor actions exhibited by tool-producing conspecif ics. More rudimentary social processes such as stimulus or local enhancement (Galef, 1988; Heyes, 1994), as demon strated in our choice experiment mentioned above, could hidden prey. Juveniles may also learn about particular Pan danus tool shapes from inspecting abandoned tools or tool counterparts in leaves, without ever observing another bird manufacturing a tool. In other words, the hypothesis of a tool culture is compatible with various social transmission mechanisms, ranging from elaborate cognitive properties to better-known and widespread learning processes. We have monitored radio-tagged wild crows from 2005 of life, foraging often in close association with parents, siblings, and other individuals. This period of dependency prior to natal dispersal could provide opportunities for social spring), obliquely (from the parental to other members of the different ages). There are also very suggestive observations quently using the same tools (Hunt, 2000b; Sarsby, 1998). results from a complex interplay of heritable predispositions, possibly) the acquisition of socially-transmitted informa contributions of these different mechanisms.

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Tool-related Cognition 10 with novel problems (i.e., those not typically encountered in behaviour or choose at random. Choice of the correct tools in novel tasks would at least indicate that the natural behav concepts, although, depending on the task, choice could be governed by previously learned associations between par ticular tools and success or by an understanding of the rela tionship between tool dimensions and task demands. Wild chimpanzees use tools of different dimensions for different tasks (e.g., Boesch & Boesch, 1990, 1993; Hicks, Fouts, & Fouts, 2005; Nishida, 1972). This has been taken task demands (Boesch & Boesch, 1993; Visalberghi, 1993). However, since the chimpanzees were not described as solv ing novel ( Gorilla gorilla ) and orangutans ( Pongo pygmaeus ) appro priately chose the longer of two tools to rake in a food re ward when it was distant and chose randomly between the tools when the reward was close (Mulcahy, Call, & Dunbar, 2005; see also Pouydebat, Berge, Gorce, & Coppens, 2005), as did a Tonkean macaque ( Macaca tonkeana ) in a similar ously chose the thinner of two sticks when necessary (An did not spontaneously choose longer tools when food was further away (Tebbich & Bshary, 2004). In Tebbich and chose short tools, and across all trials the length of the tools expected by chance (Tebbich & Bshary, 2004). A relevant question is, therefore, whether New Caledo nian crows can choose tools of appropriate dimensions and food at different depths inside a transparent, horizontal 20 trials and the longest available tool on 10 trials (both sig analysis of the data reveals that, excluding all trials in which tance to food (Figure 8; Spearman rank correlation; for Betty Deployment of Tool-oriented Behaviour The fact that at least some aspects of New Caledonian crows’ tool-oriented behaviour develop from unlearned, her itable predispositions does not imply that TOB must be ste reotyped or unrelated to reasoning in adult crows. Consider again our earlier analogy with the development of human language. A prevalent view argues that there is an inherited basis for the mechanisms of human language acquisition (Vargha-Khadem, Gadian, Copp, & Mishkin, 2005; but see Fitch, Hauser, & Chomsky, 2005), but it would be unreason able to maintain that cognition is absent from conversation. Tools are an unusual way of interacting with the physical world. Therefore, independent investigation is necessary to explore the cognitive underpinnings of TOB deployment derstanding of how the world works and why it works in the way it does” (Povinelli, 2000, p. 9). It is worth noting that, while tool use may be favoured by the pre-existence of a high level of understanding (as some argue for humans; e.g., Wolpert, 2003), the same behaviour, whatever its con trol mechanism, may promote the evolutionary development understanding the causal basis of interactions between ob arrow of causality. Another possibility is that exposure to promotes the development of folk physics and that this ten adaptation responsible for the unique level of tool use. ing hitherto unpublished re-analyses of data, and then we consider whether crows may possess anything worthy of the Choosing Tools & Clayton, 2004b; Lefebvre, Reader, & Sol, 2004; Reader, alter one’s behaviour if circumstances change (John Maynard Keynes famously replied to a fellow parliamentarian who I change my mind. What do you do, sir?”). Particularly di agnostic of intelligence is the ability to alter one’s behaviour adaptively to cope best with the change in circumstances. Therefore, s/he can choose the best tool out of a selection of tools of different dimensions when the task is varied. If tool use is based on rigid rules for choosing particular tools in particu lar situations, then we would expect that, when confronted

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Tool-related Cognition 11 Figure 8. The shortest tool chosen at each food distance by two subjects (‘Abel’: black circles, solid line; ‘Betty’: red squares, dashed line) in a length selection experiment. Trend lines are linear regressions, and the data for Abel are pooled over the two experiments he participated in. In the original above random: those of the tool whose length matched the distance to food and those of the longest tool. As the bias towards choosing the longest available tool might obscure a sensitivity to distance to food, here we exclude all such choices (15 trials for Abel and 10 for Betty). Data are replot ted from Figures 2 and 4, pages 74 and 76, “Tool Selectivity in a Non-mammal, the New Caledonian Crow (Corvus mon eduloides),” by J. Chappell and A. Kacelnik, Animal Cogni tion, 5, 71-78. Copyright 2002 by Springer-Verlag. Adapted with permission. [who participated in only one experiment], N = 7, r S = 0.764, p < 0.05; for Abel [who participated in two experiments], on pooled results from both experiments N = 10, r S = 0.652, p < 0.05]). select tools of the appropriate width. Here, a tool could be inserted through a hole of three possible diameters to dis lodge a food reward (Chappell & Kacelnik, 2004). In the diameters (1 mm less than the diameter of the three holes) bundle, or two tied together and one free. Betty showed a strong preference for the tool with the smallest diameter, to the point of dismantling the bundle to retrieve it even when a suitable tool was freely available. That she would incur this additional handling cost suggests selectivity (she strongly were suitable, but she did not use them). In a control condi tion, where all the tools were available and suitable for foodretrieval, Betty showed the same preference, suggesting that ergonomic factors. The previous test was concerned with tool use , but we also conducted experiments to investigate aspects of our crows’ tool manufacture. Both Betty and Abel were tested together on the same apparatus as used for the width-selectivity test, but with access to raw materials for tool manufacture (an making tools. Out of 30 trials, the male (Abel) retrieved food on 13 and the female (Betty) on 16 (the remaining trial was (without modifying it) in 13 trials, only making an inappro priate tool on 1 trial (the tool was narrow enough, but too short to dislodge the food). Betty retrieved food using the suitably narrow, and on 4 of these she made another tool that pell & Kacelnik, 2004). Strikingly, 16 of the 24 tools made in middleand large-hole trials would have been too thick if used on small-hole trials, whereas only one tool made in the narrow-hole trials was too thick (and it was subsequently in this task (as opposed to making exclusively narrow tools that are functional for all three hole diameters), but a post hoc analysis of one aspect of the results not examined in the original publication reveals a potential and perhaps nonobvious association between tool manufacture and foraging the trial) showed no trend with hole diameter, this latency decreased with diameter of the manufactured tool (only to success’ [transformed by reciprocal square root] as the dependent variable, tool diameter as a continuous explana for tool diameter, F 1,18 = 7.95, p F 1,18 = 0.04, p = 0.848, F 1,24 = 0.18, p = 0.671]. This is consistent only when required since the narrower the desired tool diam -

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Tool-related Cognition 12 the requisite search time until a suitable twig is found. Thus, crows seem capable of manufacturing appropriately-sized tools from raw materials as well as of choosing from a set of available tools according to the present needs, although their choice may also be constrained by inherent preferences, whether these are the product of previous learning or simply ergonomic limits. amined how two free-living New Caledonian crows made container—either a vertical box with a transparent side, or opaque vertical holes in a tree stump. Food was placed at one of two depths, which varied between blocks of trials. Agrianome fairmairei , provided alive or dead; see Figure 5, top panel) and used mainly leaf stems to extract them, while the other manufactured Pandanus tools to extract supplied lumps of attempted to extract food (this tool tended to be shorter than the distance to food in the deeper holes), and only after fail or select longer tools. Therefore, there was no evidence that ing tools, although they did adapt their behaviour once the tools had been tried. The authors argue that this demonstrated egy to solve tool problems” (Hunt, Rutledge, et al., 2006, p.307)—namely, initially using default behaviour and modi fying this appropriately following failure. They argue that mediate causal inference’ to solve the problem and that the et al., 2006). These observations contrast with those of Chappell and Kacelnik (2002, 2004) described above, who found selectiv cal differences between the studies preclude direct compari sons. Of particular relevance is the fact that the study by Hunt, Rutledge, et al. (2006) used free-living crows and a naturalistic foraging task. Consequently, experimental trials were embedded within a natural foraging context, where the crows (presumably) routinely used tools. Free-living birds are likely to develop a preference for using a tool length that is supported by our own ongoing work on stick-tool use in wild crows. If this is the case, crows may have approached the task in Hunt, Rutledge, et al.’s experiment with their de Figure 9. (a) Maximum diameter of the functional region (distal 9 cm) of the manufactured tool plotted against the diameter of the hole, in a diameter-manufacture experiment. Horizontal jitter has been added to separate overlapping data points. The blue line represents a linear regression 4, page 125, “Selection of Tool Diameter by New Caledo nian Crows Corvus moneduloides,” by J. Chappell and A. Kacelnik, Animal Cognition, 7, 121-127. Copyright 2004 by Springer-Verlag. Adapted with permission. (b) Latency to food retrieval plotted against the maximum diameter of the functional region of the manufactured tool for two subjects (Abel: black circles; Betty: red squares). Only trials where cessfully are included. Note that the statistical analysis was performed on transformed latencies (see text for details), whereas the untransformed data are plotted here for ease of interpretation. Unpublished data from Experiment 2, “Se lection of Tool Diameter by New Caledonian Crows Cor vus moneduloides,” by J. Chappell and A. Kacelnik, Animal Cognition, 7, 121-127.

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Tool-related Cognition 13 fault behaviour, not noticing that it required a different kind et al.’s terminology). In contrast, in Chappell and Kacel nik’s laboratory studies, experimental trials represented the and the novel nature of the task (the distance to food var ied between consecutive trials, rather than between blocks of trials, and food was presented in a highly distinct, novel apparatus) may have elicited case-by-case decision making. The nature of the apparatus (vertical opaqueor partiallyprovides a possible explanation for the different results. The exposed their ability to discriminate before choosing the ini tial tools because they simply were not able to assess the distance to food in vertical, opaque, or semi-opaque holes. Other methodological differences hamper comparisons. For instance, Hunt, Rutledge, et al.’s study used two food depths in separate blocks of trials, whereas Chappell and Kacelnik’s in randomly interspersed trials. These disparities highlight the former are irreplaceable for investigating ecological rel state and experience and demonstrate abilities that may or may not be important under natural circumstances. No doubt, both approaches are necessary to elucidate detailed mechanisms of learning and choice. In conclusion, New Caledonian crows, like some tool-us ing primates, are able to select appropriate tools for novel tasks. In the laboratory, they make and use tools from a va riety of materials, including (their own moulted) feathers, cardboard, and wood chips, and they readily use any elon strips of plastic, or wire (Kacelnik, Chappell, Weir, & Ken ward, 2006; personal observations). Appropriate selection of tools based on length has not as yet been demonstrated for wild crows (Hunt, Rutledge, et al., 2006), or in a similar ex periment in captivity with the other avian stick-tool user— controlled by logical inference and planning, their presence could have a rich repertoire of previous associations between tools of particular dimensions and holes of a certain depth or diameter, which would enable them to choose correctly facturing of tools conditional in size or shape on the task being faced—raises the question of which cognitive mecha nisms are employed in TOB, but it is not, per se to identify any particular ability that excludes conventional processes such as associative learning plus generalisation. Understanding? As mentioned in the introduction, humans possess intui erates, incorporating a variety of principles (such as gravity, force, connectivity, weight) that allow us to operate as obli gate tool users in a materially complex environment and to this can be described as causal understanding of the physi cal world, it need not equate to formal understanding in any 12 years of age, children (who presumably have experience affect the balance of a lever (for many, a novel task) (Amsel, Goodman, Savoie, & Clark, 1996), yet they lack a formal understanding of the underlying principles (that the mass multiplied by the distance must be equal on both sides of the fulcrum) until this is explicitly taught (Stephen Barlow, per sonal communication). Likewise, through experience most people have an implicit knowledge of what makes an effec tive hammer. If one forgets to bring a hammer on a camping similarities. This same rationale—a task requiring transfer of concepts derived from past experience to a novel prob lem—can be used to attempt to assess causal understanding in non-humans. To test for causal understanding, two main experimen between different tools (where effective tools share a com different), or between different actions with a tool (such as pushing or pulling a tool, or choosing which side of an ap with the task or tools transformed in a manner which alters the causality of the problem. Transformations are typically rules’ ( sensu acteristics of the apparatus (such as colour, shape, texture) will behave in one way, whereas those that have formed a concept about how the apparatus functions (for example, that the tool needs to be connected to the food in order to act on it) will behave in another way. However, since the num is a relatively high chance that they will perform correctly by chance. Therefore, a robust study requires either a large transformations to be used. Furthermore, the limited number of options and trials make one-trial learning very plausible, -

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Tool-related Cognition 14 mance. For example, in a task with only two options a winstay lose-shift strategy would lead to perfect performance The second approach focuses on the animals’ spontane choices, they are placed in a situation where they have a low probability of solving a task by chance alone (for example, in a hook making task an animal may be given a piece of of shapes, but only a small subset of these shapes would be expected to depend on trial-and-error and, therefore, to fol low a gradual pattern of acquisition similar to that in clas sical operant shaping experiments (e.g., Thorndike, 1898). The absence of insight should lead to gradual performance improvement because success is achieved following a se perspective) could be the critical element. In contrast, sub rely on random exploration until success but then infer the reasons for success and organise their future behaviour to wards this goal, hence improving in a more step-wise pattern. ties in formulating null hypotheses and their respective prob manufacturing a hook-shaped instrument to extract a reward by chance alone?), and in comparing performances across species. Animals differ in their behavioural repertoires and, therefore, in their likelihood of solving given experimen tal tasks (cows, for example, seem unlikely candidates for bending wire into hooks, despite reports to the contrary by a British newspaper; Townsend, 2005). Both approaches, therefore, have their advantages and should be seen as complementary, but the limitations of each of them should be taken into account when interpreting re sults. We will return to the issue of what conclusions can be drawn from such work in Section 6. We now turn our atten tion to the performance of New Caledonian crows and other can be deduced from these results regarding the presence of physical understanding. The Trap-tube Test The most widely applied test for causal understanding in the physical domain is the trap-tube task (Visalberghi & Li mongelli, 1994). In its simplest form, it consists of a trans part of the tube, the food falls into the hole and becomes move the food across the central part of an active tube, but should show no such bias when faced with an inactive tube. In some experiments another transfer test has been used, where post-training the trap is positioned off-centre to test for use of a distance-based associative rule (e.g., Limongelli, Boysen, & Visalberghi, 1995). The only New Caledonian crow tested to date (Betty) did not instantly solve the task, but instead she improved gradu ally. After around 60 trials, she spontaneously developed a herself and the food) until its distal end protruded from the opposite side, then walking to the opposite side and pulling the stick so as to extract the food in a controlled manner. eliminating the danger of another crow snatching the food, an event that could occur when pushing the food out of the opposite side of the tube. Using a combination of this tech nique and a standard pulling action (pulling the food towards her from the side closest to the food), she reached criterion (obtaining the food on 8 or more trials in three consecutive sessions of 10 trials) after 110 trials (Movie 5; Chappell & Kacelnik, 2007; Kacelnik et al., 2006). This time to acqui sition is comparable to that of chimpanzees (Limongelli et al., 1995; Reaux & Povinelli, 2000), capuchins (Visalberghi Bshary, 2004) tested on the same task, but comparability is When the trap was switched to the inactive state, Betty con tinued to avoid it using her technique, even though it was now irrelevant. Chimpanzees (Reaux & Povinelli, 2000) and capuchins (Visalberghi & Limongelli, 1994) also continue to avoid the inactive trap, and consequently it has been argued that they do not understand the causal basis of the task. In iour in the transfer test (Tebbich, Taborsky, Fessl, Dvorak, & Winkler, 2004). Two chimpanzees and a capuchin monkey have been tested with the off-centre trap design, following that she was probably using a distance-based associative rule, whereas the two chimpanzees remained highly success ful (Limongelli et al., 1995). Interesting as it is to compare performance levels across species, the conclusions that can be drawn from this general experimental design are limited (Chappell, 2006). One cave at is that it is not clear what the cognitive implications are of failure to revert to random insertion after the trap is inverted (Machado & Silva, 2003). Although logically it is not neces there is no cost to doing so (as in most published experiments)

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Tool-related Cognition 15 no incentive to modify their behaviour. Interestingly, even humans continue to avoid the inverted trap, despite their un derstanding of the physical principles involved (Silva, Page, & Silva, 2005). It is equally hard to draw conclusions from do revert to random tool inser had learned through reinforcement the characteristics of the stimulus (i.e., the tube with downward-oriented trap) so spe and they react as if in a completely new task, to which they monitor the moment-to-moment movement of the food with respect to the trap; if the trap is inverted, the food will never randomly. This is thought to account for the performance (Tebbich et al., 2004). There are similar problems with the off-centre trap test. Although below-chance performance in rule, above-chance performance does not mean that they un derstood the causal basis of the task. They might have been food away from the trap,’ without any understanding as to why they should do this. To solve problems associated with the standard task, Nicky Clayton and colleagues (Seed, Tebbich, Emery, & Clayton, 2006; Tebbich, Seed, Emery, & Clayton, in press) developed an alternative task to test the same principle, but which could also be used by non-tool-using species—in Figure 10. derstanding in rooks. Tubes A-B were used in both Tebbich et al. (2007) and Seed et al. (2006), whereas tubes C-D were only used by Seed et al. (2006). The arrow shows the path the food will take if the stick is pulled in the correct direc tion. For further explanation, see text. From Figure 2, page 699, “Investigating Physical Cognition in Rooks, Corvus frugilegus,” by A. M. Seed, S. Tebbich, N. J. Emery, and N. S. Clayton, Current Biology, 16, 697-701. Copyright 2006 by Elsevier Ltd. Adapted with permission. their experiments, rooks. To adapt the task to non-tool-users, wooden dowels with two solid transparent disks attached (with the food reward positioned between them) were preIn the study by Tebbich et al. (in press), following training to pull the dowel out of a plain, horizontal tube to get food, on this task were then tested with a tube where food was had to move the food over the latter trap and out the mouth of the tube; in the other (Tube B), one trap was again blocked at the bottom by a black disc, but the second trap was open, so food could be retrieved by pulling the dowel towards the trap with no base, upon which the food would fall clear of the apparatus. In both tube types, therefore, the active trap terion performance (after 30, 40, and 50 trials) on the singletrap tube, but all remained at chance throughout testing with both two-trap tubes. Seed et al. (2006) tested a separate group of eight rooks in a very similar manner. Crucially however, they did not A were tested on Tube B, and vice versa). All 7 rooks were pected by chance over 20 trials. These results are consistent could also be explained by learning to avoid traps with black discs at the bottom. To exclude the latter possibility, further transfer tests were administered (see Figure 10). In Tube C, one trap was blocked at the top and the other one had no base, and both ends of the tube were blocked by bungs; food end of the stick disappeared into the bung and could not be pulled out again. Tube D had the same traps but no bungs in the ends of the tube; however, the apparatus was lowered to the ground such that food could only be extracted by pulling over the trap with the blocked top. These tubes were designed so that the stimuli that previously signalled which direction

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Tool-related Cognition 16 responding on the basis of a single associatively-learned cue to two blocks of ten trials of Tube C, followed by two blocks While appropriately cautious of conclusions based on a sessed either an understanding of the observable forces in volved, or had abstracted the rules of the task (see also Chap pell, 2006). However, success on any one task, particularly about cues that were causally-relevant for that task. For ex ample, Guillem could have learned that two cues predicted towards the trap with the black disc on the top; and pull the food towards a trap that has no black disc, if there is space underneath the tube. The striking individual differences in performance (only 3 of 7 rooks learned to solve the original trap-tube task in Tebbich et al., in press, and none passed the the transfer tasks in Seed et al., 2006) make this possibil ity more plausible, since if rooks were predisposed to form theories about physical causality, we would expect more of them to demonstrate this ability in the experiments. It is worth comparing this work with that on capuchin monkeys. The performance of capuchin monkeys seems to be based almost entirely on trial-and-error learning of procedural rules (Visalberghi & Limongelli, 1994; Visalberghi & Trin ca, 1989). In some experiments, chimpanzees have shown greater sensitivity to the causally-relevant aspects of the tasks (e.g., Limongelli et al., 1995; Visalberghi, Fragaszy, & Savage-Rumbaugh, 1995), but these successful perfor mances fall short of demonstrating an understanding of the physical mechanisms involved (see Povinelli, 2000). Sensi tivity to functionally-relevant features of tools has also been demonstrated by a series of experiments by Marc Hauser and colleagues, primarily with non-tool-using cotton-top tamarins ( Saguinus oedipus; Hauser, 1997; Hauser, Kralik, & Botto-Mahan, 1999; Hauser, Pearson, & Seelig, 2002; Hauser, Santos, Spaepen, & Pearson, 2002; Santos, Rosati, Sproul, Spaulding, & Hauser, 2005), but also by testing rhe sus macaques ( Macaca mulatta; Santos, Miller, & Hauser, 2003), common marmosets ( Callithrix jacchus; Spaulding & Hauser, 2005), and vervet monkeys ( Cercopithecus ae thiops; Santos, Pearson, Spaepen, Tsao, & Hauser, 2006). relevant in certain situations, rather than an understanding of underlying causality (Penn & Povinelli, 2007). Indeed, in recent experiments Santos and colleagues have tested tamarins on experiments similar to those used by Povinelli and colleagues with chimpanzees (Povinelli, 2000) and ap parently found that like chimpanzees, the tamarins failed to distinguish between the functional and non-functional tools or actions (reviewed by Hauser & Santos, in press). In conclusion, the result from these experiments, and oth between tools or discrete actions (e.g., Povinelli, 2000, chap. 4-10; Visalberghi & Trinca, 1989), have yielded, at best, very limited evidence for understanding of physical causality in non-humans. Hook Making As discussed above, another technique for investigating non-humans’ understanding of physical causality is to ob serve their problem-solving behaviour in situations that are examined how New Caledonian crows manipulate pliant material to form functional tools. This line originates from an unplanned observation in an experiment where Betty and another crow, Abel, faced a choice between a straight or a hooked piece of garden wire, with food available in a small bucket at the bottom of a verti cal transparent tube (Weir, 2006). The goal was to extend the 4.1) to include tool shape in addition to length and diameter. The apparatus was designed such that the hooked wire was functional for retrieval of the bucket, but the straight wire was not (this last restriction proved to be almost, but not off with it to another part of the aviary before retrieving the bucket. Betty attempted to lift the bucket with the straight wire, and when this proved ineffective, proceeded to bend it into a hook, which she used to extract the bucket (Fig ure 11; Weir, Chappell, & Kacelnik, 2002). Although this has become a textbook example of animal intelligence (e.g., Barnard, 2004; Boyd & Silk, 2006; Freeman, 2002) and was animal” in a recent review of bird cognition (Emery, 2006, p. 32; note that Emery wrote this before the publication of the results of Seed et al., 2006), unravelling the cognitive processes behind it presents serious challenges. Perhaps the crucial issue is whether Betty’s wire-bending demonstrates causal understanding. In 10 trials following the initial observation, Betty was only given a straight wire and the distal end of it (i.e., the end not held in her beak) using wire and pulling laterally from the proximal end (Weir et al., 2002). The bent part at the distal end formed the hook. (Note

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Tool-related Cognition 17 Figure 11. A crow in the Oxford laboratory (Betty) uses a hook—which she has just made by bending a piece of wire— to extract a bucket with food from the bottom of a well (Weir et al., 2002). The images do not come from the same trial. Photos: Alex Weir (reprinted with permission). bent piece of metal that could function to pull the bucket out of the well; we recognise that, as pointed out by Emery, 2006, in several cases the angle of the bend was less than 90 degrees.) Betty had been wild-caught as an immature bird two years before the experiment took place, so her experi ence before entering captivity is unknown, but we are not aware of any natural materials that could be bent and used like garden wire. To our knowledge, Betty had never expe cleaners a year before this experiment (which she was not seen to bend or use as tools). In subsequent experiments, Betty was presented with the these attempted probes declined rapidly (the median duration bends, following her previous techniques (Weir & Kacelnik, 2006), but because of the properties of the new material she was unsuccessful. (The strips could not be wedged in a sub strate in the same manner as the wire.) Betty then developed a new technique, proximal bending, that was more effective with the aluminium and which she used on all subsequent occasions (Figure 12a; Movie 7). This involved bending the end of the strip that was held in her beak, rather than the dis tal end as previously. A consequence of this technique was the tool, so the instrument needed to be turned around before end of the strip whilst holding the hooked end. terms of causal understanding is not straightforward. One approach is to ask what behaviour we would expect from an agent capable solely of trial-and-error learning. Such an (Weir et al., 2002) that a certain sequence of actions with the be wedged, then the proximal end pulled at an angle at the distal end, then the wire removed and inserted into the tube and used to pull up the bucket. Since the new task and mate rial closely resembled the old one, we would expect such an agent to perform initially the same series of actions—which is indeed what we observed with Betty. Following failure of this sequence, the agent’s behaviour should become more ringer, Kornell, & Olufs, 2001), but in a (relatively) random upon manipulating the shape of the tool, rather than on other components of the previously-successful sequence, such as the tool insertion or lifting action. Therefore, it seems that Betty’s bending actions were to some extent goal directed in that she was intent on produc had some understanding of how to make a hook, since she so. In other words, in both experiments she was able to in -

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Tool-related Cognition 18 vent a method of shaping the material into a functional and probably preconceived form. However, these results suffer results. We are, therefore, unable to quantify the statistical problem in the investigation of creative behaviour. Betty’s repeated attempts to use the wrong end of the why a hook was needed— certainly, an agent who fully un derstood the task should never probe with the wrong end of the tool. However, we should be cautious about leaping performance since humans do sometimes make similar mis takes despite undoubtedly possessing sophisticated folk physics (discussed in more detail later in this section). It is also interesting to note that chimpanzees only correctly re reoriented a straight tool (Povinelli, Reaux, Theall, & Giam brone, 2000b, Experiment 16 conditions E and G). Figure 12. Tools used by a captive crow (Betty) during experiments where she had to (a) make hooks (by bending the tool); (b) make the tool narrower (by squeezing or unbending it); or (c) make the tool longer (by unbending it) to retrieve food are on the right. Scale bar is 3 cm. Photos: Alex Weir (reprinted with permission). We tested Betty’s understanding of the relationship be tween tool-shape and success with two additional brief experiments involving more radical transformations of the strip was pre-bent at both ends, preventing it from being in serted through a narrow hole—an action which was neces sary to dislodge food. Betty did modify the tool and obtain food on the only valid trial (in two trials she managed to retrieve food without modifying the tool), although we can both ends of the tool (Figure 12b), which may have been for ergonomic reasons (ease of holding) rather than a purpose hole). In the second experiment, the aluminium strip was pro vided pre-bent into a broad U-shape, which was too short for the task; it had to be lengthened by unbending to retrieve food from a horizontal tube. Betty unbent the tool and ob tained the food on two of the three valid trials (again, Betty retrieved food on one trial in a non-anticipated manner; Fig -

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Tool-related Cognition 19 Betty died before completing more replicates, and the small number of trials together with the variability in her behaviour (to be expected in this kind of experiment) precludes statisti cal analysis. However, it is important to note that she never performed a bending action in these tasks, even though this had been the behaviour consistently deployed and rewarded by reasoning’ cannot be asserted, it is reasonable to doubt forcement history, bending was not her generalised response to inaccessible food and manipulable material (Figure 12). Although Betty did not show a human-level understand ing of the causal need for a hook, her degree of conceptu alisation of the problem seems to exceed that previously documented in other animals. Of particular relevance are a panzees (Povinelli, Reaux, Theall, & Giambrone, 2000a). In these studies, 7 chimpanzees were each given 12 trials where they had to unbend a tool to retrieve the reward, in bent the tool when it was necessary to do so, and she did so (to bend the tool). Moreover, when only one end of the tool insert the wrong end into the apparatus throughout the test ing period. These results suggest that chimpanzees can learn (in this case through explicit provision of information) the properties of tools while remaining ignorant of the abstract concepts involved in successful tool use. derstanding does not conform to a presence/absence dichot omy. Some anecdotal observations with humans may serve to illustrate this point. We recently presented our research on New Caledonian crows at the Royal Society of London’s stall—adults and teenagers, including many Fellows of the Royal Society and even its most recent past President (Fig ure 13)—to participate in an informal experiment resembling opportunity to extract souvenir badges from a vertical, trans parent tube, using a pair of pliers (to simulate a crow’s beak) and a piece of straight wire or aluminium strip. We explained that the goal of the task was to extract the badge, and most visitors had seen video footage of Betty’s successful wire bending. Surprisingly, and like Betty had done during early trials, a substantial proportion of people attempted to retrieve the reward without modifying the starting material—an ap proach that was only successful in a small fraction of at tempts. Many other participants produced an exaggerated hook with a U-shaped tip that was unsuitable for the desired suitable hook—probably imitating Betty—but then inserted the straight, non-functional end into the tube! This exercise had a pedagogical and slightly humorous intention, and is hardly a rigorous test of humans’ ability on this task. Yet, de likely knowledge of the pliability of wire, many humans did not deduce the utility of a hook or design it correctly before Figure 13. A human subject (‘Bob’) attempts to replicate Betty’s wire-bending task (see Figure 11). On the left Betty (mounted) illustrates the original behaviour. Both Betty and ‘Charles’ respectively). Photo: Alex Kacelnik (reprinted with permission). engaging in some practical testing. In humans as in crows, it seems that performance on physical tasks may not always be based on a strong form of a priori understanding, but that understanding may in fact be promoted by some practical engagement with the task itself (a similar point was made by Hunt, Rutledge, et al., 2006). Concluding Remarks Betty’s manufacture of hooks from novel materials and our knowledge, amongst the closest any non-humans have However, as we have mentioned earlier, the concept of un lows we examine at greater length some of the issues raised by this word and their implications for comparative cogni tion research. In the earlier description of Betty’s wire-bending behav -

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Tool-related Cognition 20 ing the material into a functional and probably preconceived be no need to look beyond associative learning and generali sation, albeit of a relatively complex and unlikely nature. We chose the original wording partly as a teaser (surely some readers’ reservations about anthropomorphic language must have been aroused by the sentence) and partly because, in our opinion, this possibility is worth entertaining as a work ing hypothesis. We adhere to the spirit of Morgan’s Canon (Thomas, 2001), and certainly do not argue that, because Betty acted as a human might, she did so on the same con & Giambrone, 2000). However, to dismiss the possibility of higher cognition out-of-hand could be construed as anthro pocentric in itself (Keeley, 2004). On the basis of the avail able evidence, we cannot yet exclude the possibility that all apparently intelligent behaviours shown by New Caledonian crows can be explained by associative learning mechanisms, and the same may be true for other non-human species. Giv en this situation, is it still meaningful or useful to refer to understanding in crows and in animal behaviour in general? depth by philosophers (e.g., Overskeid, 2005; Searle, 1980), and there is still no general agreement about how it should about X to be an obstacle to reaching a relevant, currently active goal” (Overskeid, 2005, p. 601), which implies that understanding is a default state, and most animals (including lysing situations in which humans would claim that they did or did not understand something, a process which—while entirely valid from a philosophical point of view—necessar is unsuitable for application in animal cognition research. ers by observing whether they behave appropriately in cer tain situations; if so, we can ascribe to them some degree of understanding in the relevant domain. For example, if someone anticipates rain and prepares herself by carrying an umbrella, Overskeid would infer that she had some under in an environment where the weather could be predicted by simple, reliable cues, and she was genetically endowed with rules that enabled accurate weather prediction, it would seem inappropriate to ascribe any degree of understanding to her, regardless of her successful performance (indeed, plants what derstands or the correctness of her understanding. In the domain of folk physics, when we say that an ani that they have some (more-or-less correct) knowledge of the causal basis of the task (Vonk, 2005). However, this intro one of which is associative learning, and there is no uni versal agreement on how to separate associatively-learned knowledge from associatively-learned behaviour . Equally, most humans have only a limited, proximate understanding of the causal basis of phenomena around them, including their actions. For instance, one can say that the reason im ages disappeared from the TV screen is because the set was the images to be formed. Thus, a pertinent question is how accurate and detailed causal understanding needs to be for us to recognise it as such. We do not have a precise answer We believe, however, that progress is possible if one relaxes research, while avoiding over-interpreting results. The role of theory in this case resembles that of evolutionary assump advances. our interest in the wider implications of our research. New Caledonian crows and other corvids exhibit behaviour that tions cry out for comparative work with other seemingly in telligent animals, notably humans and other primates. Such comparisons are important and have produced some striking examples of convergent evolution in birds and mammals. Empirical evidence for corvid intelligence is accumulating 2004, p. 182; see also Clayton & Emery, 2005). We naturally share the general enthusiasm for corvid research but think that care needs to be taken when interpreting and describing results. In particular, we need to be cautious of ascribing gen eral cognitive abilities to the whole Corvidae family based investigations have demonstrated that they are equipped

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Tool-related Cognition 21 mechanisms (e.g., Bugnyar & Heinrich, 2005; Dally, Emery, & Clayton, 2005, 2006; Emery & Clayton, 2001). Similarly, Gymnorhinus cyanocephalus ) are highly social, and can use transitive reasoning to predict the dominance of Whilst it is possible that these abilities are equivalent to the similar cognitive processes in humans and are shared by the whole Corvidae family, it could equally be the case that they ented behaviour of New Caledonian crows may be another example of such an adaptation. In contrast, many of these cognitive abilities appear to be found in all species of great ape (Tomasello & Call, 1997) and are exhibited in a wide variety of different contexts, making it more plausible that eral’ intelligence. However, in many ways corvid research is still decades behind primate research, particularly in terms at this stage (a point also made by others, e.g., Emery, 2006; Emery & Clayton, 2004a). We have recently attempted to identify possible evolution ary origins of the behavioural action patterns that lead to tool use in New Caledonian crows (Kenward et al., 2007). Thom as Bugnyar and co-workers from Austria had documented in that does not habitually use tools in the wild, but is otherwise renowned for its cognitive capacities (Bugnyar & Heinrich, 2005; Heinrich, 1999). Taking advantage of the fact that the Austrian and the Oxford research groups had employed similar (albeit not identical) observation protocols for their oriented behaviours between the two species. Our analyses revealed striking developmental similarities between TOB in crows and food-caching behaviour in ravens, including simi lar precursor behaviours. Given that the common ancestor of New Caledonian crows and ravens was almost certainly a caching species (de Kort & Clayton, 2006), we hypothesise that the action patterns for tool use in crows have their evo lutionary origins in caching behaviour. Tool use in New Caledonian crows is the result of natu ral selection, yet we remain largely ignorant of the selective forces that may have fostered this unusual behaviour in the evolutionary past and those that maintain it under presentday conditions. In 2005 we launched a long-term research our colleagues from New Zealand, will inform experimen tal work with captive crows. This concerted work in the lab were unable to address in this review. References A lcock, J. (1972). The evolution of the use of tools by feed ing animals. Evolution, 26 , 464-473. Amsel, E., Goodman, G., Savoie, D., & Clark, M. (1996). The development of reasoning about causal and non Child Development, 67 , 1624-1646. Anderson, J. R., & Henneman, M. C. (1994). Solutions to a tool-use problem in a pair of Cebus apella . Mammalia, 58 , 351-361. Andersson, S. (1989). Tool use by the fan-tailed raven (Cor vus rhipidurus). Condor, 91 , 999. Barnard, C. J. (2004). Animal behaviour: Mechanism, devel opment, function and evolution Beck, B. B. (1980). Animal tool behavior: The use and man ufacture of tools by animals. Beck, B. B. (1986). Tools and intelligence. In R. J. Hoage & L. Goldman (Eds.), Animal intelligence: Insights into the animal mind Smithsonian Institution Press. Biro, D., Inoue-Nakamura, N., Tonooka, R., Yamakoshi, G., Sousa, C., & Matsuzawa, T. (2003). Cultural innova Animal Cognition, 6 , 213-223. Blaisdell, A. P., Sawa, K., Leising, K. J., & Waldmann, M. R. (2006). Causal reasoning in rats. Science, 311 , 10201022. Boesch, C., & Boesch, H. (1990). Tool use and tool making in wild chimpanzees. Folia Primatologica, 54 , 86-99. Boesch, C., & Boesch, H. (1993). Diversity of tool use and tool-making in wild chimpanzees. In A. Berthelet & J. Chevaillon (Eds.), T he use of tools by human and nonhuman primates Press. Borsari, A., & Ottoni, E. B. (2005). Preliminary observations of tool use in captive hyacinth macaws ( Anodorhynchus hyacinthinus ). Animal Cognition, 8 , 48-52. Boswall, J. (1978). Further notes on tool using by birds and related behaviour. Avicultural Magazine, 84 , 162-166. Boswall, J. (1983). Tool-using and related behaviour by Avicultural Magazine, 89 , 94-108. Boyd, R., & Silk, J. B. (2006). How humans evolved (4th Bugnyar, T., & Heinrich, B. (2005). Ravens, Corvus corax, differentiate between knowledgeable and ignorant com petitors. Proceedings of the Royal Society of London B, 272 , 1641-1646. can Crow. Wilson Bulletin, 112 , 283-284. Call, J. (2004). Inferences about the location of food in the great apes ( Pan paniscus , Pan troglodytes , Gorilla go rilla , and Pongo pygmaeus ). Journal of Comparative

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