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.     

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.

     

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.     

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.     

Strong between‐site variation in New Caledonian crows’ use of hook‐tool‐making materials

Functional tool use requires the selection of appropriate raw materials. New Caledonian crows Corvus moneduloides are known for their extraordinary tool‐making behaviour, including the crafting of hooked stick tools from branched vegetation. We describe a surprisingly strong between‐site difference in the plant materials used by wild crows to manufacture these tools: crows at one study site use branches of the non‐native shrub Desmanthus virgatus, whereas only approximately 7 km away, birds apparently ignore this material in favour of the terminal twigs of an as‐yet‐unidentified tree species. Although it is likely that differences in local plant communities drive this striking pattern, it remains to be determined how and why crows develop such strong site‐specific preferences for certain raw materials.     

Context-dependent ‘safekeeping’ of foraging tools in New Caledonian crows

Several animal species use tools for foraging, such as sticks to extract embedded arthropods and honey, or stones to crack open nuts and eggs. While providing access to nutritious foods, these behaviours may incur significant costs, such as the time and energy spent searching for, manufacturing and transporting tools. These costs can be reduced by re-using tools, keeping them safe when not needed. We experimentally investigated what New Caledonian crows do with their tools between successive prey extractions, and whether they express tool ‘safekeeping’ behaviours more often when the costs (foraging at height), or likelihood (handling of demanding prey), of tool loss are high. Birds generally took care of their tools (84% of 176 prey extractions, nine subjects), either trapping them underfoot (74%) or storing them in holes (26%)—behaviours we also observed in the wild (19 cases, four subjects). Moreover, tool-handling behaviour was context-dependent, with subjects: keeping their tools safe significantly more often when foraging at height; and storing tools significantly more often in holes when extracting more demanding prey (under these conditions, foot-trapping proved challenging). In arboreal environments, safekeeping can prevent costly tool losses, removing a potentially important constraint on the evolution of habitual and complex tool behaviour.     

Design complexity in termite-fishing tools of chimpanzees (Pan troglodytes)

Adopting the approach taken with New Caledonian crows (Corvus moneduloides), we present evidence of design complexity in one of the termite-fishing tools of chimpanzees (Pan troglodytes) in the Goualougo Triangle, Republic of Congo. Prior to termite fishing, chimpanzees applied a set of deliberate, distinguishable actions to modify herb stems to fashion a brush-tipped probe, which is different from the form of fishing tools used by chimpanzees in East and West Africa. This means that ‘brush-tipped fishing probes’, unlike ‘brush sticks’, are not a by-product of use but a deliberate design feature absent in other chimpanzee populations. The specialized modifications to prepare the tool for termite fishing, measures taken to repair non-functional brushes and appropriate orientation of the modified end suggest that these wild chimpanzees are attentive to tool modifications. We also conducted experimental trials that showed that a brush-tipped probe is more effective in gathering insects than an unmodified fishing probe. Based on these findings, we suggest that chimpanzees in the Congo Basin have developed an improved fishing probe design.     

Cognitive Processes Associated with Sequential Tool Use in New Caledonian Crows

Background

Using tools to act on non-food objects—for example, to make other tools—is considered to be a hallmark of human intelligence, and may have been a crucial step in our evolution. One form of this behaviour, ‘sequential tool use’, has been observed in a number of non-human primates and even in one bird, the New Caledonian crow (Corvus moneduloides). While sequential tool use has often been interpreted as evidence for advanced cognitive abilities, such as planning and analogical reasoning, the behaviour itself can be underpinned by a range of different cognitive mechanisms, which have never been explicitly examined. Here, we present experiments that not only demonstrate new tool-using capabilities in New Caledonian crows, but allow examination of the extent to which crows understand the physical interactions involved.

Methodology/Principal Findings

In two experiments, we tested seven captive New Caledonian crows in six tasks requiring the use of up to three different tools in a sequence to retrieve food. Our study incorporated several novel features: (i) we tested crows on a three-tool problem (subjects were required to use a tool to retrieve a second tool, then use the second tool to retrieve a third one, and finally use the third one to reach for food); (ii) we presented tasks of different complexity in random rather than progressive order; (iii) we included a number of control conditions to test whether tool retrieval was goal-directed; and (iv) we manipulated the subjects'' pre-testing experience. Five subjects successfully used tools in a sequence (four from their first trial), and four subjects repeatedly solved the three-tool condition. Sequential tool use did not require, but was enhanced by, pre-training on each element in the sequence (‘chaining’), an explanation that could not be ruled out in earlier studies. By analyzing tool choice, tool swapping and improvement over time, we show that successful subjects did not use a random probing strategy. However, we find no firm evidence to support previous claims that sequential tool use demonstrates analogical reasoning or human-like planning.

Conclusions/Significance

While the ability of subjects to use three tools in sequence reveals a competence beyond that observed in any other species, our study also emphasises the importance of parsimony in comparative cognitive science: seemingly intelligent behaviour can be achieved without the involvement of high-level mental faculties, and detailed analyses are necessary before accepting claims for complex cognitive abilities.     

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.     

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.     

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.     

On the evolutionary and ontogenetic origins of tool‐oriented behaviour in New Caledonian crows (Corvus moneduloides)

New Caledonian crows (Corvus moneduloides) are prolific tool users in captivity and in the wild, and have an inherited predisposition to express tool‐oriented behaviours. To further understand the evolution and development of tool use, we compared the development of object manipulation in New Caledonian crows and common ravens (Corvus corax), which do not routinely use tools. We found striking qualitative similarities in the ontogeny of tool‐oriented behaviour in New Caledonian crows and food‐caching behaviour in ravens. Given that the common ancestor of New Caledonian crows and ravens was almost certainly a caching species, we therefore propose that the basic action patterns for tool use in New Caledonian crows may have their evolutionary origins in caching behaviour. Noncombinatorial object manipulations had similar frequencies in the two species. However, frequencies of object combinations that are precursors to functional behaviour increased in New Caledonian crows and decreased in ravens throughout the study period, ending 6 weeks post‐fledging. These quantitative observations are consistent with the hypothesis that New Caledonian crows develop tool‐oriented behaviour because of an increased motivation to perform object combinations that facilitate the necessary learning. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 870–877.     

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.     

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.     

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.     

Extreme convergence in stick insect evolution: phylogenetic placement of the Lord Howe Island tree lobster

The ‘tree lobsters’ are an enigmatic group of robust, ground-dwelling stick insects (order Phasmatodea) from the subfamily Eurycanthinae, distributed in New Guinea, New Caledonia and associated islands. Its most famous member is the Lord Howe Island stick insect Dryococelus australis (Montrouzier), which was believed to have become extinct but was rediscovered in 2001 and is considered to be one of the rarest insects in the world. To resolve the evolutionary position of Dryococelus, we constructed a phylogeny from approximately 2.4 kb of mitochondrial and nuclear sequence data from representatives of all major phasmatodean lineages. Our data placed Dryococelus and the New Caledonian tree lobsters outside the New Guinean Eurycanthinae as members of an unrelated Australasian stick insect clade, the Lanceocercata. These results suggest a convergent origin of the ‘tree lobster’ body form. Our reanalysis of tree lobster characters provides additional support for our hypothesis of convergent evolution. We conclude that the phenotypic traits leading to the traditional classification are convergent adaptations to ground-living behaviour. Our molecular dating analyses indicate an ancient divergence (more than 22 Myr ago) between Dryococelus and its Australian relatives. Hence, Dryococelus represents a long-standing separate evolutionary lineage within the stick insects and must be regarded as a key taxon to protect with respect to phasmatodean diversity.     

Diversification and cumulative evolution in New Caledonian crow tool manufacture

Many animals use tools but only humans are generally considered to have the cognitive sophistication required for cumulative technological evolution. Three important characteristics of cumulative technological evolution are: (i) the diversification of tool design; (ii) cumulative change; and (iii) high-fidelity social transmission. We present evidence that crows have diversified and cumulatively changed the design of their pandanus tools. In 2000 we carried out an intensive survey in New Caledonia to establish the geographical variation in the manufacture of these tools. We documented the shapes of 5550 tools from 21 sites throughout the range of pandanus tool manufacture. We found three distinct pandanus tool designs: wide tools, narrow tools and stepped tools. The lack of ecological correlates of the three tool designs and their different, continuous and overlapping geographical distributions make it unlikely that they evolved independently. The similarities in the manufacture method of each design further suggest that pandanus tools have gone through a process of cumulative change from a common historical origin. We propose a plausible scenario for this rudimentary cumulative evolution.     

Rooks perceive support relations similar to six-month-old babies

Some corvids have demonstrated cognitive abilities that rival or exceed those of the great apes; for example, tool use in New Caledonian crows, and social cognition, episodic-like memory and future planning in Western scrub-jays. Rooks appear to be able to solve novel tasks through causal reasoning rather than simple trial-and-error learning. Animals with certain expectations about how objects interact would be able to narrow the field of candidate causes substantially, because some causes are simply ‘impossible’. Here we present evidence that rooks hold such expectations and appear to possess perceptual understanding of support relations similar to that demonstrated by human babies, which is more comprehensive than that of chimpanzees.     

Is primate tool use special? Chimpanzee and New Caledonian crow compared

The chimpanzee (Pan troglodytes) is well-known in both nature and captivity as an impressive maker and user of tools, but recently the New Caledonian crow (Corvus moneduloides) has been championed as being equivalent or superior to the ape in elementary technology. I systematically compare the two taxa, going beyond simple presence/absence scoring of tool-using and -making types, on four more precise aspects of material culture: (i) types of associative technology (tools used in combination); (ii) modes of tool making; (iii) modes of tool use; and (iv) functions of tool use. I emphasize tool use in nature, when performance is habitual or customary, rather than in anecdotal or idiosyncratic. On all four measures, the ape shows more variety than does the corvid, especially in modes and functions that go beyond extractive foraging. However, more sustained field research is required on the crows before this contrast is conclusive.     

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.