Oscillatory extraction behaviour suggests functional attributes of crows' hooked-stick tools.

New Caledonian crows are the only nonhuman animals known to craft hooked-sticks for use in foraging. Since their first description over 25 years ago, researchers have been unable to provide a detailed account of how these complex tools function in natural probe sites. Using close-up video footage, we document how a New Caledonian crow operated a hooked-stick to extract a large tree weta from a chamber in a tree trunk. The extraction technique had two distinct, separate components: (1) simultaneous oscillating head rotation and reciprocating bill action, and (2) measured pulling with the tool. Analysis of this first detailed field observation of hooked-stick use suggests a link between hooked-stick tool characteristics, functionality and skilled manipulation in natural prey extraction by these technological birds. Our findings also provide a rare, if not novel, example of tool-associated oscillatory manipulation in nonhuman animals.

Purifying Selection in Corvids Is Less Efficient on Islands.

Theory predicts that deleterious mutations accumulate more readily in small populations. As a consequence, mutation load is expected to be elevated in species where life-history strategies and geographic or historical contingencies reduce the number of reproducing individuals. Yet, few studies have empirically tested this prediction using genome-wide data in a comparative framework. We collected whole-genome sequencing data for 147 individuals across seven crow species (Corvus spp.). For each species, we estimated the distribution of fitness effects of deleterious mutations and compared it with proxies of the effective population size Ne. Island species with comparatively smaller geographic range sizes had a significantly increased mutation load. These results support the view that small populations have an elevated risk of mutational meltdown, which may contribute to the higher extinction rates observed in island species.

A genome-wide investigation of adaptive signatures in protein-coding genes related to tool behaviour in New Caledonian and Hawaiian crows.

Very few animals habitually manufacture and use tools. It has been suggested that advanced tool behaviour co-evolves with a suite of behavioural, morphological and life history traits. In fact, there are indications for such an adaptive complex in tool-using crows (genus Corvus species). Here, we sequenced the genomes of two habitually tool-using and ten non-tool-using crow species to search for genomic signatures associated with a tool-using lifestyle. Using comparative genomic and population genetic approaches, we screened for signals of selection in protein-coding genes in the tool-using New Caledonian and Hawaiian crows. While we detected signals of recent selection in New Caledonian crows near genes associated with bill morphology, our data indicate that genetic changes in these two lineages are surprisingly subtle, with little evidence at present for convergence. We explore the biological explanations for these findings, such as the relative roles of gene regulation and protein-coding changes, as well as the possibility that statistical power to detect selection in recently diverged lineages may have been insufficient. Our study contributes to a growing body of literature aiming to decipher the genetic basis of recently evolved complex behaviour.

New Caledonian crows' basic tool procurement is guided by heuristics, not matching or tracking probe site characteristics.

Contrasting findings made it unclear what cognitive processes New Caledonian crows use to procure suitable tools to solve tool tasks. Most previous studies suggested that their tool procurement is achieved by either trial and error or a simple heuristic. The latter provides a fast and cognitively efficient method for stable, routinized behaviour based on past experience with little or no deliberate decision-making. However, early papers by Chappell and Kacelnik reported that two New Caledonian crows procured tools after closely assessing the tool characteristics required for the task, thus using deliberate decision-making, or a 'customized strategy'. Here, I tested eight New Caledonian crows to determine their default behaviour in basic tool procurement tasks as a check on whether or not they use customized strategies. I used two rigorous experiments closely based on Chappell and Kacelnik's experiments. The crows did not use a customized strategy in either experiment, but their behaviour was clearly consistent with tool procurement predominantly guided by a familiarity heuristic. I discuss potential methodological issues that may have led to different conclusions in Chappell and Kacelnik's studies. Heuristic-guided, routinized behaviour in tool procurement has potential implications for understanding how standardization occurs in the early evolution of complex tool manufacture, both in New Caledonian crows and early humans.

New Caledonian crows afford invaluable comparative insights into human cumulative technological culture.

The New Caledonian crow may be the only non-primate species exhibiting cumulative technological culture. Its foraging tools show clear signs of diversification and progressive refinement, and it seems likely that at least some tool-related information is passed across generations via social learning. Here, we explain how these remarkable birds can help us uncover the basic biological processes driving technological progress.

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.

Spontaneous metatool use by New Caledonian crows.

A crucial stage in hominin evolution was the development of metatool use -- the ability to use one tool on another [1, 2]. Although the great apes can solve metatool tasks [3, 4], monkeys have been less successful [5-7]. Here we provide experimental evidence that New Caledonian crows can spontaneously solve a demanding metatool task in which a short tool is used to extract a longer tool that can then be used to obtain meat. Six out of the seven crows initially attempted to extract the long tool with the short tool. Four successfully obtained meat on the first trial. The experiments revealed that the crows did not solve the metatool task by trial-and-error learning during the task or through a previously learned rule. The sophisticated physical cognition shown appears to have been based on analogical reasoning. The ability to reason analogically may explain the exceptional tool-manufacturing skills of New Caledonian crows.

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.

Tool-making New Caledonian crows have large associative brain areas.

Animals with a high rate of innovative and associative-based behavior usually have large brains. New Caledonian (NC) crows stand out due to their tool manufacture, their generalized problem-solving abilities and an extremely high degree of encephalization. It is generally assumed that this increased brain size is due to the ability to process, associate and memorize diverse stimuli, thereby enhancing the propensity to invent new and complex behaviors in adaptive ways. However, this premise lacks firm empirical support since encephalization could also result from an increase of only perceptual and/or motor areas. Here, we compared the brain structures of NC crows with those of carrion crows, jays and sparrows. The brains of NC crows were characterized by a relatively large mesopallium, striatopallidal complex, septum and tegmentum. These structures mostly deal with association and motor-learning. This supports the hypothesis that the evolution of innovative or complex behavior requires a brain composition that increases the ability to associate and memorize diverse stimuli in order to execute complex motor output. Since apes show a similar correlation of cerebral growth and cognitive abilities, the evolution of advanced cognitive skills appears to have evolved independently in birds and mammals but with a similar neural orchestration.

Extraordinary large brains in tool-using New Caledonian crows (Corvus moneduloides).

A general correlation exists between brain weight and higher cognitive ability in birds and mammals. In birds this relationship is especially evident in corvids. These animals are well-known for their flexible behavior and problem-solving abilities, and have relatively large brains associated with a pallial enlargement. At the behavioral level, New Caledonian crows stand out amongst corvids because of their impressive object manipulation skills both in the wild and in the laboratory. However, nothing is known about the relative size of their brains. Here we show that NC crows have highly encephalised brains relative to most other birds that have been studied. We compared the relative brain size of five NC crows with combined data for four passerine species (7 European carrion crows, 2 European magpies, 3 European jays and 4 domestic sparrows) and found that NC crows had significantly larger brains. A comparison only with the seven carrion crows also revealed significantly larger brains for NC crows. When compared with brain data for 140 avian species from the literature, the NC crow had one of the highest degrees of encephalisation, exceeding that of the 7 other Corvidae in the data set.

Habitual tool use innovated by free-living New Zealand kea.

The emergence of flexible tool use is rare in the animal kingdom and thought to be largely constrained by either cognitive ability or ecological factors. That mostly birds with a high level of intelligence innovate tool use in captivity is consistent with the former hypothesis. We report here the first documented case of habitual tool use innovated in the wild by a bird species only known to have used tools in captivity. Trap-boxes containing food-bait and snap-trap(s) were installed in the remote Murchison Mountains, New Zealand, from 2002 to catch introduced stoats. Kea tampered with the trap-boxes in various ways. Over approximately 2.5 years, sticks were found inserted into at least 227 different trap-boxes that were up to 27 km apart. Video footage confirmed that the stick insertion was kea tool use. Trap-boxes are unlikely to have provided the only possibility for kea tool use in their habitat given their extractive foraging and skilled object manipulation. We argue that they instead greatly facilitated the opportunity for tool use, thus increasing the chance that kea would invent the behaviour. The innovation of tool use by kea in response to facilitation provides rare field support for the cognitive constraints hypothesis.

Corvid Technologies: How Do New Caledonian Crows Get Their Tool Designs?

Recent research shows that New Caledonian crows can incorporate information from researcher-made objects into objects they subsequently manufacture. This 'mental template matching' is one of several possible - mutually compatible - mechanisms for the cultural transmission of tool designs among wild crows.

Design complexity and strength of laterality are correlated in New Caledonian crows' pandanus tool manufacture.

Population-level laterality is generally considered to reflect functional brain specialization. Consequently, the strength of population-level laterality in manipulatory tasks is predicted to positively correlate with task complexity. This relationship has not been investigated in tool manufacture. Here, we report the correlation between strength of laterality and design complexity in the manufacture of New Caledonian crows' three pandanus tool designs: wide, narrow and stepped designs. We documented indirect evidence of over 5,800 tool manufactures on 1,232 pandanus trees at 23 sites. We found that the strength of laterality in tool manufacture was correlated with design complexity in three ways: (i) the strongest effect size among the population-level edge biases for each design was for the more complex, stepped design, (ii) the strength of laterality at individual sites was on average greater for the stepped design than it was for the simpler wide and narrow, non-stepped designs, and (iii) there was a positive, but non-significant, trend for a correlation between the strength of laterality and the number of steps on a stepped tool. These three aspects together indicate that greater design complexity generally elicits stronger lateralization of crows' pandanus tool manufacture.

Adaptive bill morphology for enhanced tool manipulation in New Caledonian crows.

Early increased sophistication of human tools is thought to be underpinned by adaptive morphology for efficient tool manipulation. Such adaptive specialisation is unknown in nonhuman primates but may have evolved in the New Caledonian crow, which has sophisticated tool manufacture. The straightness of its bill, for example, may be adaptive for enhanced visually-directed use of tools. Here, we examine in detail the shape and internal structure of the New Caledonian crow's bill using Principal Components Analysis and Computed Tomography within a comparative framework. We found that the bill has a combination of interrelated shape and structural features unique within Corvus, and possibly birds generally. The upper mandible is relatively deep and short with a straight cutting edge, and the lower mandible is strengthened and upturned. These novel combined attributes would be functional for (i) counteracting the unique loading patterns acting on the bill when manipulating tools, (ii) a strong precision grip to hold tools securely, and (iii) enhanced visually-guided tool use. Our findings indicate that the New Caledonian crow's innovative bill has been adapted for tool manipulation to at least some degree. Early increased sophistication of tools may require the co-evolution of morphology that provides improved manipulatory skills.

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.

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.

Perineuronal satellite neuroglia in the telencephalon of New Caledonian crows and other Passeriformes: evidence of satellite glial cells in the central nervous system of healthy birds?

Glia have been implicated in a variety of functions in the central nervous system, including the control of the neuronal extracellular space, synaptic plasticity and transmission, development and adult neurogenesis. Perineuronal glia forming groups around neurons are associated with both normal and pathological nervous tissue. Recent studies have linked reduction in the number of perineuronal oligodendrocytes in the prefrontal cortex with human schizophrenia and other psychiatric disorders. Therefore, perineuronal glia may play a decisive role in homeostasis and normal activity of the human nervous system. Here we report on the discovery of novel cell clusters in the telencephala of five healthy Passeriforme, one Psittaciform and one Charadriiforme bird species, which we refer to as Perineuronal Glial Clusters (PGCs). The aim of this study is to describe the structure and distribution of the PGCs in a number of avian species. PGCs were identified with the use of standard histological procedures. Heterochromatin masses visible inside the nuclei of these satellite glia suggest that they may correspond to oligodendrocytes. PGCs were found in the brains of nine New Caledonian crows, two Japanese jungle crows, two Australian magpies, two Indian mynah, three zebra finches (all Passeriformes), one Southern lapwing (Charadriiformes) and one monk parakeet (Psittaciformes). Microscopic survey of the brain tissue suggests that the largest PGCs are located in the hyperpallium densocellulare and mesopallium. No clusters were found in brain sections from one Gruiform (purple swamphen), one Strigiform (barn owl), one Trochiliform (green-backed firecrown), one Falconiform (chimango caracara), one Columbiform (pigeon) and one Galliform (chick). Our observations suggest that PGCs in Aves are brain region- and taxon-specific and that the presence of perineuronal glia in healthy human brains and the similar PGCs in avian gray matter is the result of convergent evolution. The discovery of PGCs in the zebra finch is of great importance because this species has the potential to become a robust animal model in which to study the function of neuron-glia interactions in healthy and diseased adult brains.

Population genetic structure and colonisation history of the tool-using New Caledonian crow.

New Caledonian crows exhibit considerable variation in tool making between populations. Here, we present the first study of the species' genetic structure over its geographical distribution. We collected feathers from crows on mainland Grande Terre, the inshore island of Toupéti, and the nearby island of Maré where it is believed birds were introduced after European colonisation. We used nine microsatellite markers to establish the genotypes of 136 crows from these islands and classical population genetic tools as well as Approximate Bayesian Computations to explore the distribution of genetic diversity. We found that New Caledonian crows most likely separate into three main distinct clusters: Grande Terre, Toupéti and Maré. Furthermore, Toupéti and Maré crows represent a subset of the genetic diversity observed on Grande Terre, confirming their mainland origin. The genetic data are compatible with a colonisation of Maré taking place after European colonisation around 1900. Importantly, we observed (1) moderate, but significant, genetic differentiation across Grande Terre, and (2) that the degree of differentiation between populations on the mainland increases with geographic distance. These data indicate that despite individual crows' potential ability to disperse over large distances, most gene flow occurs over short distances. The temporal and spatial patterns described provide a basis for further hypothesis testing and investigation of the geographical variation observed in the tool skills of these crows.

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.

Social learning in New Caledonian crows.

New Caledonian (NC) crows are the most sophisticated tool manufacturers other than humans. The diversification and geographical distribution of their three Pandanus tool designs that differ in complexity, as well as the lack of ecological correlates, suggest that cumulative technological change has taken place. To investigate the possibility that high-fidelity social transmission mediated this putative ratchet-like process, we studied the ontogeny of Pandanus tool manufacture and social organization in free-living NC crows. We found that juvenile crows took more than 1 year to reach adult proficiency in their Pandanus tool skills. Although trial-and-error learning is clearly important, juveniles have ample opportunity to learn about Pandanus tool manufacture by both observing their parents and interacting with artifactual material. The crows' social system seems likely to promote the faithful social transmission of local tool designs by both favoring the vertical transmission of tool information and minimizing horizontal transmission. We suggest that NC crows develop their Pandanus tool skills in a highly scaffolded learning environment that facilitates the cumulative technological evolution of tool designs.