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.     

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.     

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.     

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.     

Foraging Ontogeny is not Linked to Delayed Maturation in Squirrel Monkeys (Saimiri sciureus)

The acquisition of complex foraging behaviors by young is a proposed cause of a prolonged juvenile phase in many vertebrates, including primates. I compared the foraging behaviors of infant, juvenile and adult squirrel monkeys to determine if significant age‐related differences in foraging behavior and efficiency were present. Infants and juveniles differed from each other in patterns of prey and fruit foraging, but few differences existed between juveniles and adults. Despite differing in the use of foraging substrates, young juveniles (8–12 mo) were as efficient as older juveniles (1–4 yr) and adults at capturing and processing large prey. Young juveniles (<1 yr) were limited in their ability to consume husked palm fruits due to an inability to peel them to obtain pulp. By 1 yr of age, however, foraging behaviors of adults and juveniles were nearly indistinguishable. The absence of meaningful differences between adults and juvenile foraging is not consistent with the hypothesis that the need to develop foraging skills accounts for the pattern of extended juvenility in squirrel monkeys.     

Do New Caledonian crows solve physical problems through causal reasoning?

The extent to which animals other than humans can reason about physical problems is contentious. The benchmark test for this ability has been the trap-tube task. We presented New Caledonian crows with a series of two-trap versions of this problem. Three out of six crows solved the initial trap-tube. These crows continued to avoid the trap when the arbitrary features that had previously been associated with successful performances were removed. However, they did not avoid the trap when a hole and a functional trap were in the tube. In contrast to a recent primate study, the three crows then solved a causally equivalent but visually distinct problem--the trap-table task. The performance of the three crows across the four transfers made explanations based on chance, associative learning, visual and tactile generalization, and previous dispositions unlikely. Our findings suggest that New Caledonian crows can solve complex physical problems by reasoning both causally and analogically about causal relations. Causal and analogical reasoning may form the basis of the New Caledonian crow's exceptional tool skills.     

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.     

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.     

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.

     

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.     

Foraging behavior predicts age at independence in juvenile Eurasian dippers (Cinclus cinclus)

Timing of foraging independence may be controlled by parents,offspiing, or both and may have consequences for dispersal,reproduction, and survival In a study of juvenile Eurasian dippers(Cinclus cinchus), I examined the relationship between individualdifferences in parental provisioning, the development of foraging,and the timing of independence. Young dippers forage very differentlyfrom adults, specializing on small, stationary pre such as simuliidlarvae (Diptera), and avoiding energetically costly and highlyskilled foraging techniques, such as diving, by which adultsobtain larger prey In my Welsh study area, age at independencevaried substantially within and between broods. Juveniles thatrelied more on simuliids and less on larger prey were independentsooner, as were juveniles with higher rates of intake whileforaging the effect was obvious 3–4 days after fledging.Provisioning rate and total caloric intake over the dependentperiod was unrelated to age at independence, although greaterreliance on parental feeding was associated with higher totalcaloric intake. Higher rates of intake from begging were correlatedwith reduced foraging time. The results demonstrate that theacquisition of the adult foraging strategy is not a prerequisitefor independence or, hence, dispersal. In fact, mastering theskills necessary to capture larger prey may delay independence.Individual juvenile dippers seem to find different solutionsto the trade-off between gaining sufficient food (either frombegging or from foraging for simuliids) and the eventual necessityof learning to forage like an adult.     

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.     

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.     

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.     

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.     

Recruitment calling: a novel form of extended parental care in an altricial species

In many altricial birds, fledglings disperse when they are no longer fed, and this dispersal marks the end of parental care. In some species, however, young remain in close association with their parents after nutritional independence. Because juveniles are still inferior foragers at this stage, they might benefit from parental assistance in locating good feeding sites, but this possibility remains largely unexplored. Here, we show that parents and helpers in pied babbler (Turdoides bicolor) societies use a recruitment call to direct nutritionally independent, but inexperienced, foragers to particular food patches. Observations and a playback experiment indicated that adult babblers use a "purr" call to recruit group members to a foraging patch. Creation of experimental foraging patches supported observations that individuals tend to give the call when they are foraging on abundant, divisible food sources and when their group contains independent fledglings (youngsters who are no longer fed directly). Fledglings responded to calls more often than adults, who frequently encountered aggression from the caller if they did, and the fledglings gained significant foraging benefits. This is the first study to demonstrate that altricial birds may use recruitment calls to extend parental care past the period of direct provisioning.     

Do naive juvenile seabirds forage differently from adults?

Foraging skills of young individuals are assumed to be inferior to those of adults. The reduced efficiency of naive individuals may be the primary cause of the high juvenile mortality and explain the deferment of maturity in long-lived species. However, the study of juvenile and immature foraging behaviour has been limited so far. We used satellite telemetry to compare the foraging movements of juveniles, immatures and breeding adult wandering albatrosses Diomedea exulans, a species where foraging success is positively influenced by the distance covered daily. We showed that juveniles are able to use favourable winds as soon as the first month of independence, but cover shorter distances daily and spend more time sitting on water than adults during the first two months after fledging. These reduced movement capacities do not seem to be the cause of higher juvenile mortality. Moreover, juveniles almost never restrict their movement to specific areas, as adults and immatures frequently do over shelf edges or oceanic zones, which suggest that the location of appropriate areas is learned through experience. Immatures and adults have equivalent movement capacities, but when they are central place foragers, i.e. when adults breed or immatures come to the colony to display and pair, immatures make shorter trips than adults. The long duration of immaturity in this species seems to be related to a long period of learning to integrate the foraging constraints associated with reproduction and central place foraging. Our results indicate that foraging behaviour of young albatrosses is partly innate and partly learned progressively over immaturity. The first months of learning appear critical in terms of survival, whereas the long period of immaturity is necessary for young birds to attain the skills necessary for efficient breeding without fitness costs.     

Nest and foraging‐site selection in Yellowhammers Emberiza citrinella: implications for chick provisioning

Capsule Vegetation structure and invertebrate abundance interact to influence both foraging sites and nestling provisioning rate; when invertebrate availability is low, adults may take greater risks to provide food for their young.

Aims To investigate nesting and foraging ecology in a declining farmland bird whose fledging success is influenced by the availability of invertebrate prey suitable for feeding to offspring, and where perceived predation risk during foraging can be mediated by vegetation structure.

Methods Provisioning rates of adult Yellowhammers feeding nestlings were measured at nests on arable farmland. Foraging sites were compared with control sites of both the same and different microhabitats; provisioning rate was related to habitat features of foraging‐sites.

Results Foraging sites had low vegetation density, probably enhancing detection of predators, or high invertebrate abundance at high vegetation density. Parental provisioning rate decreased with increasing vegetation cover at foraging sites with high invertebrate abundance; conversely, where invertebrate abundance was low, provisioning rate increased with increasing vegetation cover.

Conclusions Vegetation structure at foraging sites suggests that a trade‐off between predator detection and prey availability influences foraging site selection in Yellowhammers. Associations between parental provisioning rate and vegetation variables suggest that where invertebrate abundance is high birds increase time spent scanning for predators at higher vegetation densities; however, when prey are scarce, adults may take more risks to provide food for their young.     

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.     

Body condition influences ontogeny of foraging behavior in juvenile southern elephant seals

Ontogeny of diving and foraging behavior in marine top predators is poorly understood despite its importance in population recruitment. This lack of knowledge is partly due to the difficulties of monitoring juveniles in the wild, which is linked to high mortality early in life. Pinnipeds are good models for studying the development of foraging behaviors because juveniles are large enough to robustly carry tracking devices for many months. Moreover, parental assistance is absent after a juvenile departs for its first foraging trip, minimizing confounding effects of parental input on the development of foraging skills. In this study, we tracked 20 newly weaned juvenile southern elephant seals from Kerguelen Islands for up to 338 days during their first trip at sea following weaning. We used a new generation of satellite relay tags, which allow for the transmission of dive, accelerometer, and location data. We also monitored, at the same time, nine adult females from the colony during their post‐breeding trips, in order to compare diving and foraging behaviors. Juveniles showed a gradual improvement through time in their foraging skills. Like adults females, they remarkably adjusted their swimming effort according to temporal changes in buoyancy (i.e., a proxy of their body condition). They also did not appear to exceed their aerobic physiological diving limits, although dives were constrained by their smaller size compared to adults. Changes in buoyancy appeared to also influence their decision to either keep foraging or return to land, alongside the duration of their haul outs and choice of foraging habitat (oceanic vs. plateau). Further studies are thus needed to better understand how patterns in juveniles survival, and therefore elephant seal populations, might be affected by their changes in foraging skills and changes in their environmental conditions.