Context-dependent tool use in New Caledonian crows

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

Lateralized tool use in wild New Caledonian crows

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

New Caledonian crows plan for specific future tool use

The ability to plan for future events is one of the defining features of human intelligence. Whether non-human animals can plan for specific future situations remains contentious: despite a sustained research effort over the last two decades, there is still no consensus on this question. Here, we show that New Caledonian crows can use tools to plan for specific future events. Crows learned a temporal sequence where they were (a) shown a baited apparatus, (b) 5 min later given a choice of five objects and (c) 10 min later given access to the apparatus. At test, these crows were presented with one of two tool–apparatus combinations. For each combination, the crows chose the right tool for the right future task, while ignoring previously useful tools and a low-value food item. This study establishes that planning for specific future tool use can evolve via convergent evolution, given that corvids and humans shared a common ancestor over 300 million years ago, and offers a route to mapping the planning capacities of animals.     

Cognitive requirements for tool use by New Caledonian crows (Corvus moneduloides)

Abstract

Cumulative technological evolution has been suggested to explain the existence of different pandanus tool designs manufactured by New Caledonian crows. Circumstantial evidence from the distribution of the three tool designs that they manufacture suggests transmission of the designs probably involves accurate social learning, a characteristic considered essential for the cumulative evolution of tools. Recently, Kenward et al. (2005) reported that four hand‐raised crows developed basic stick tool use without social learning. This finding cast doubt on the importance of social learning in the evolution of crows’ pandanus tools in the wild. Here, we report that a naïve male crow at Parc Zoo‐Forestier, Nouméa, developed proficient stick tool use without social input in 2002. In 2004, four captive crows, including the naïve male, that were inexperienced with pandanus material were given an opportunity to use and/or manufacture pandanus tools. Only two of the four birds used the tools but none manufactured tools. Our preliminary findings and the work with the four hand‐raised crows keep open the possibility that the evolution of crows’ pandanus tool designs is based on social learning. We propose that social learning and a disposition to develop basic tool use without social input are both essential cognitive requirements for cumulative technological evolution.     

Gourmand New Caledonian crows munch rare escargots by dropping

Numerous broken shells of a rare endemic snail Placostylus fibratus, a species rated as vulnerable, were scattered around rocky beds of dry creeks in rainforest of New Caledonian. We set a video camera near one site to identify the predator. We recorded a New Caledonian crow Corvus moneduloides dropping and consuming the snail. This is the first direct evidence of the crow dropping of this native species. The assumed weight of snails relative to the crow is exceptionally heavy among prey dropped by birds.     

Activity profiles and hook-tool use of New Caledonian crows recorded by bird-borne video cameras

New Caledonian crows are renowned for their unusually sophisticated tool behaviour. Despite decades of fieldwork, however, very little is known about how they make and use their foraging tools in the wild, which is largely owing to the difficulties in observing these shy forest birds. To obtain first estimates of activity budgets, as well as close-up observations of tool-assisted foraging, we equipped 19 wild crows with self-developed miniature video cameras, yielding more than 10 h of analysable video footage for 10 subjects. While only four crows used tools during recording sessions, they did so extensively: across all 10 birds, we conservatively estimate that tool-related behaviour occurred in 3% of total observation time, and accounted for 19% of all foraging behaviour. Our video-loggers provided first footage of crows manufacturing, and using, one of their most complex tool types—hooked stick tools—under completely natural foraging conditions. We recorded manufacture from live branches of paperbark (Melaleuca sp.) and another tree species (thought to be Acacia spirorbis), and deployment of tools in a range of contexts, including on the forest floor. Taken together, our video recordings reveal an ‘expanded’ foraging niche for hooked stick tools, and highlight more generally how crows routinely switch between tool- and bill-assisted foraging.     

Parallel tool industries in New Caledonian crows

Individual specialization in the use of foraging tools occurs in hunter-gatherer societies but is absent in non-human primate tool use. 'Parallel tool industries' in hunter-gatherers are mainly based on strict sexual division of labour that is highly reliant on social conformity. Here, we show that 12 individuals in a population of New Caledonian crows on Maré Island had strong preferences for either stick tools or pandanus tools. Eight of the 12 crows had exclusive preferences. The individual specialization that we found is probably associated with different foraging niches. However, in spite of sexual size dimorphism there was no significant association between the sex of crows and their tool preferences. Our findings demonstrate that highly organized, strict sexual division of labour is not a necessary prerequisite for the evolution of parallel tool industries.     

The crafting of hook tools by wild New Caledonian crows

The 'crafting' of tools involves (i) selection of appropriate raw material, (ii) preparatory trimming and (iii) fine, three-dimensional sculpting. Its evolution is technologically important because it allows the open-ended development of tools. New Caledonian crows manufacture an impressive range of stick and leaf tools. We previously reported that their toolkit included hooked implements made from leafy twigs, although their manufacture had never been closely observed. We describe the manufacture of 10 hooked-twig tools by an adult crow and its dependent juvenile. To make all 10 tools, the crows carried out a relatively invariant three-step sequence of complex manipulations that involved (i) the selection of raw material, (ii) trimming and (iii) a lengthy sculpting of the hook. Hooked-twig manufacture contrasts with the lack of sculpting in the making of wooden tools by other non-humans such as chimpanzees and woodpecker finches. This fine, three-stage crafting process removes another alleged difference between humans and other animals.     

Vocal culture in New Caledonian crows Corvus moneduloides

While recent research suggests that some animal species may possess ‘cultural’ traditions, much of the current evidence for wild populations remains contentious. This is largely due to the difficulty of demonstrating a fundamental prerequisite for the existence of culture: social learning. As the only case where social learning has been demonstrated conclusively, and subsequently linked to spatial or temporal trait variation, avian vocal dialects are the best studied, and most widely accepted, form of animal culture. Here, we investigate the potential for vocal culture in one of the few animals for which material culture has been suggested: the New Caledonian crow Corvus moneduloides. We show that this species: (1) possesses the capacity for social learning of vocalizations (experimental evidence in the form of a captive subject that reproduces human speech and other anthropogenic noises); and (2) exhibits significant large‐scale, population‐level variation in its vocalizations (cross‐island playback experiments, with analyses controlling for a substantial set of potentially confounding variables). In combination, this provides strong evidence for the existence of ‘culture’ in these birds. More specifically, our findings reveal that the species exhibits sufficient social learning mechanisms, and within‐population structuring, to generate and perpetuate cultural variation in at least one behavioural domain. This is a critical first step towards demonstrating cultural transmission in other behaviours, including tool manufacture and tool use, opening the door for the simultaneous investigation of vocal and material culture in a nonhuman species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 767–776.     

The evolutionary origins and ecological context of tool use in New Caledonian crows

New Caledonian (NC) crows Corvus moneduloides are the most prolific avian tool users. In the wild, they use at least three distinct tool types to extract invertebrate prey from deadwood and vegetation, with some of their tools requiring complex manufacture, modification and/or deployment. Experiments with captive-bred, hand-raised NC crows have demonstrated that the species has a strong genetic predisposition for basic tool use and manufacture, suggesting that this behaviour is an evolved adaptation. This view is supported by recent stable-isotope analyses of the diets of wild crows, which revealed that tool use provides access to highly profitable hidden prey, with preliminary data indicating that parents preferentially feed their offspring with tool-derived food. Building on this work, our review examines the possible evolutionary origins of these birds’ remarkable tool-use behaviour. Whilst robust comparative analyses are impossible, given the phylogenetic rarity of animal tool use, our examination of a wide range of circumstantial evidence enables a first attempt at reconstructing a plausible evolutionary scenario. We suggest that a common ancestor of NC crows, originating from a (probably) non-tool-using South-East Asian or Australasian crow population, colonised New Caledonia after its last emersion several million years ago. The presence of profitable but out-of-reach food, in combination with a lack of direct competition for these resources, resulted in a vacant woodpecker-like niche. Crows may have possessed certain behavioural and/or morphological features upon their arrival that predisposed them to express tool-use rather than specialised prey-excavation behaviour, although it is possible that woodpecker-like foraging preceded tool use. Low levels of predation risk may have further facilitated tool-use behaviour, by allowing greater expenditure of time and energy on object interaction and exploration, as well as the evolution of a ‘slow’ life-history, in which prolonged juvenile development enables acquisition of complex behaviours. Intriguingly, humans may well have influenced the evolution of at least some of the species’ tool-oriented behaviours, via their possible introduction of candlenut trees together with the beetle larvae that infest them. Research on NC crows’ tool-use behaviour in its full ecological context is still in its infancy, and we expect that, as more evidence accumulates, some of our assumptions and predictions will be proved wrong. However, it is clear from our analysis of existing work, and the development of some original ideas, that the unusual evolutionary trajectory of NC crows is probably the consequence of an intricate constellation of interplaying factors.     

Complex cognition and behavioural innovation in New Caledonian crows

Apes, corvids and parrots all show high rates of behavioural innovation in the wild. However, it is unclear whether this innovative behaviour is underpinned by cognition more complex than simple learning mechanisms. To investigate this question we presented New Caledonian crows with a novel three-stage metatool problem. The task involved three distinct stages: (i) obtaining a short stick by pulling up a string, (ii) using the short stick as a metatool to extract a long stick from a toolbox, and finally (iii) using the long stick to extract food from a hole. Crows with previous experience of the behaviours in stages 1–3 linked them into a novel sequence to solve the problem on the first trial. Crows with experience of only using string and tools to access food also successfully solved the problem. This innovative use of established behaviours in novel contexts was not based on resurgence, chaining and conditional reinforcement. Instead, the performance was consistent with the transfer of an abstract, causal rule: ‘out-of-reach objects can be accessed using a tool’. This suggests that high innovation rates in the wild may reflect complex cognitive abilities that supplement basic learning mechanisms.     

Animal cognition: crows spontaneously solve a metatool task

A recent study found that tool-manufacturing New Caledonian crows spontaneously solved a metatool task in which the birds used a tool to obtain a second, longer tool that could then be used to obtain food that was otherwise out of reach.     

New Caledonian crows attend to multiple functional properties of complex tools

The ability to attend to the functional properties of foraging tools should affect energy-intake rates, fitness components and ultimately the evolutionary dynamics of tool-related behaviour. New Caledonian crows Corvus moneduloides use three distinct tool types for extractive foraging: non-hooked stick tools, hooked stick tools and tools cut from the barbed edges of Pandanus spp. leaves. The latter two types exhibit clear functional polarity, because of (respectively) a single terminal, crow-manufactured hook and natural barbs running along one edge of the leaf strip; in each case, the ‘hooks’ can only aid prey capture if the tool is oriented correctly by the crow during deployment. A previous experimental study of New Caledonian crows found that subjects paid little attention to the barbs of supplied (wide) pandanus tools, resulting in non-functional tool orientation during foraging. This result is puzzling, given the presumed fitness benefits of consistently orienting tools functionally in the wild. We investigated whether the lack of discrimination with respect to (wide) pandanus tool orientation also applies to hooked stick tools. We experimentally provided subjects with naturalistic replica tools in a range of orientations and found that all subjects used these tools correctly, regardless of how they had been presented. In a companion experiment, we explored the extent to which normally co-occurring tool features (terminal hook, curvature of the tool shaft and stripped bark at the hooked end) inform tool-orientation decisions, by forcing birds to deploy ‘unnatural’ tools, which exhibited these traits at opposite ends. Our subjects attended to at least two of the three tool features, although, as expected, the location of the hook was of paramount importance. We discuss these results in the context of earlier research and propose avenues for future work.     

New Caledonian crows learn the functional properties of novel tool types

New Caledonian crows were presented with Bird and Emery's (2009a) Aesop's fable paradigm, which requires stones to be dropped into a water-filled tube to bring floating food within reach. The crows did not spontaneously use stones as tools, but quickly learned to do so, and to choose objects and materials with functional properties. Some crows discarded both inefficient and non-functional objects before observing their effects on the water level. Interestingly, the crows did not learn to discriminate between functional and non-functional objects and materials when there was an arbitrary, rather than causal, link between object and reward. This finding suggests that the crows' performances were not based on associative learning alone. That is, learning was not guided solely by the covariation rate between stimuli and outcomes or the conditioned reinforcement properties acquired by functional objects. Our results, therefore, show that New Caledonian crows can process causal information not only when it is linked to sticks and stick-like tools but also when it concerns the functional properties of novel types of tool.     

Introduced Lantana camara used as tools by New Caledonian crows (Corvus moneduloides)

Abstract

New Caledonian crows commonly use sticks and similar plant material as hooked and non‐hooked tools to extract prey. They are known to target certain tree species that produce twigs of the right natural shape for easy conversion into tools. All previously identified species supplying tool materials have been native or endemic to New Caledonia. Here I report that crows living in disturbed habitats also use the barbed twigs of an introduced climbing plant, Lantana camara, as tools. Over an 8‐year period I collected 12 L. camara tools used by NC crows at three locations: Bourail and Sarraméa, on mainland Grande Terre, and on the island of Maré. I found these tools left in natural probe sites (Bourail and Sarraméa) or at artificial feeding sites (Maré), but I do not know if the crows targeted L. camara or simply used the closest suitable material. Nevertheless, the use of L. camara indicates that the behaviour of certain free‐living NC crows is sufficiently flexible to enable them to evaluate and use exotic plants for tool material.     

Human-like, population-level specialization in the manufacture of pandanus tools by New Caledonian crows Corvus moneduloides

The main way of gaining insight into the behaviour and neurological faculties of our early ancestors is to study artefactual evidence for the making and use of tools, but this places severe constraints on what knowledge can be obtained. New Caledonian crows, however, offer a potential analogous model system for learning about these difficult-to-establish aspects of prehistoric humans. I found new evidence of human-like specialization in crows' manufacture of hook tools from pandanus leaves: functional lateralization or 'handedness' and the shaping of these tools to a rule system. These population-level features are unprecedented in the tool behaviour of free-living non-humans and provide the first demonstration that a population bias for handedness in tool-making and the shaping of tools to rule systems are not concomitant with symbolic thought and language. It is unknown how crows obtain their tool behaviour. Nevertheless, at the least they can be studied in order to learn about the neuropsychology associated with early specialized and/or advanced population features in tool-making such as hook use, handedness and the shaping of tools to rule systems.     

Flexibility in problem solving and tool use of kea and New Caledonian crows in a multi access box paradigm

Parrots and corvids show outstanding innovative and flexible behaviour. In particular, kea and New Caledonian crows are often singled out as being exceptionally sophisticated in physical cognition, so that comparing them in this respect is particularly interesting. However, comparing cognitive mechanisms among species requires consideration of non-cognitive behavioural propensities and morphological characteristics evolved from different ancestry and adapted to fit different ecological niches. We used a novel experimental approach based on a Multi-Access-Box (MAB). Food could be extracted by four different techniques, two of them involving tools. Initially all four options were available to the subjects. Once they reached criterion for mastering one option, this task was blocked, until the subjects became proficient in another solution. The exploratory behaviour differed considerably. Only one (of six) kea and one (of five) NCC mastered all four options, including a first report of innovative stick tool use in kea. The crows were more efficient in using the stick tool, the kea the ball tool. The kea were haptically more explorative than the NCC, discovered two or three solutions within the first ten trials (against a mean of 0.75 discoveries by the crows) and switched more quickly to new solutions when the previous one was blocked. Differences in exploration technique, neophobia and object manipulation are likely to explain differential performance across the set of tasks. Our study further underlines the need to use a diversity of tasks when comparing cognitive traits between members of different species. Extension of a similar method to other taxa could help developing a comparative cognition research program.     

Hook tool manufacture in New Caledonian crows: behavioural variation and the influence of raw materials

Background

New Caledonian crows use a range of foraging tools, and are the only non-human species known to craft hooks. Based on a small number of observations, their manufacture of hooked stick tools has previously been described as a complex, multi-stage process. Tool behaviour is shaped by genetic predispositions, individual and social learning, and/or ecological influences, but disentangling the relative contributions of these factors remains a major research challenge. The properties of raw materials are an obvious, but largely overlooked, source of variation in tool-manufacture behaviour. We conducted experiments with wild-caught New Caledonian crows, to assess variation in their hooked stick tool making, and to investigate how raw-material properties affect the manufacture process.

Results

In Experiment 1, we showed that New Caledonian crows’ manufacture of hooked stick tools can be much more variable than previously thought (85 tools by 18 subjects), and can involve two newly-discovered behaviours: ‘pulling’ for detaching stems and bending of the tool shaft. Crows’ tool manufactures varied significantly: in the number of different action types employed; in the time spent processing the hook and bending the tool shaft; and in the structure of processing sequences. In Experiment 2, we examined the interaction of crows with raw materials of different properties, using a novel paradigm that enabled us to determine subjects’ rank-ordered preferences (42 tools by 7 subjects). Plant properties influenced: the order in which crows selected stems; whether a hooked tool was manufactured; the time required to release a basic tool; and, possibly, the release technique, the number of behavioural actions, and aspects of processing behaviour. Results from Experiment 2 suggested that at least part of the natural behavioural variation observed in Experiment 1 is due to the effect of raw-material properties.

Conclusions

Our discovery of novel manufacture behaviours indicates a plausible scenario for the evolutionary origins, and gradual refinement, of New Caledonian crows’ hooked stick tool making. Furthermore, our experimental demonstration of a link between raw-material properties and aspects of tool manufacture provides an alternative hypothesis for explaining regional differences in tool behaviours observed in New Caledonian crows, and some primate species.