New Caledonian Crow

= Introduction =

Tool use and its commitment to intelligence are topics of interest when analysing the sophistication of Man. The Corvid family of crows are becoming renowned for their enhanced cognitive skills with special mention of the New Caledonian crow who has an extraordinary ability to use tools to acquire otherwise unobtainable food (Mehlhorn, 2009) and ,according to Hunt (1996) and Kenward (2004) are the most ‘prolific avian tool users’. This article reviews the evidence for their proposed intelligence and explores the New Caledonian Crows usefulness as a model system to be studied in the field of Neuroscience.

= The leading non-human tool user =

The previous reports of tools use in wild birds followed only subtle modifications of materials to obtain prey whilst the NC crow can use multiple materials including twigs and the barbed leaves of the pandanus plant whilst performing specialized manipulations suited to the material (Hunt, 1996). NC crow behaviour entails the first evidence of free-living non-human hooked tool use (Hunt, 1996). Evidence of a non-human selecting a suitable raw material, trimming it and then finely crafting it into a functional prey-capturing aid breaks down a major theory of contrast between humans and other creatures. We will now discuss some of the major species competing for the title of the leading non-human tool user.

Non-human primates
Chimpanzees, who develop primitive straight twig tools (Boesch, 1996), have previously been postulated as a model for the cognitive capabilities of the earliest human tool users and were thought to be the only non-humans to extensively make and use tools in the wild (Beck 1980). However Nagel et al (1993) disputes their use as a model for early human tool use due to the lack of standardization in the final tool products and the lack of evidence suggesting an improvement in their modifications and the fact that the shape of their tools are determined more largely by the shape of the twig rather than the actions of the tool maker (Isac, 1976; Lieberman 1991). This is in contrast to the actions of NC crows whose tools (especially the stepped-cut pandanus leaf tools) require complex manipulation of the original material to derive its functionality. Also chimpanzees only need to control one variable length or diameter at a time when making their tools (Wynn &amp; McGrew 1989). Hooked-twig manufacture by NC crow exhibits a far greater level of sculpting than the making of wooden tools by chimpanzees (Hunt &amp; Gray, 2004a). Chimpanzees and oragutans lack the individual specialization in foraging tools (McGrew,1992; Van Schaik &amp; Knott, 2001). A special feature of NC crow behaviour is the ability to use two distinctive tool types in their foraging, i.e. the pandanus leaf tool and those made from sticks and similar materials (Hunt &amp; Gray,2002;Hunt&amp; Gray,2003). Often both tools will be found at the same foraging site providing evidence for the specialization of tool choice for the task at hand, enabling the capture of different prey. Gorrillas, Japanese macaques, chimpanzees and capuchin monkeys all show a weak performance in the meta-tool task compared to the NC crow. Rhesus Macaques and vervet monkeys have been demonstrated to successfully select tools based on relevant features (Santos et al 2006) but show similar limitations to the chimpanzees.

Egyptian Vultures
Egyptian Vultures, Neophron percnopterus have demonstrated the ability to select the necessary stone to throw at ostrich eggs strongly suggesting that they have a causal understanding of the relationship between the weight or size of a stone and the success in obtaining their food, at least and perhaps an appreciation for the folk physics involved in the breaking of the egg (Thouless et al, 1987).

Woodpecker Finches
Woodpecker Finches, Cactospiza pallida possess the ability to maniupluate materials (cactus spines and twigs for example ) into effective tools (Millikan &amp; Bowman, 1967; Tebbich and Bshary, 2004). When subjected to the trap tube test they appear to be solving the problem through associative learning also (Tebbich and Bshary, 2004).

Cotton-top tamarins
Cotton-top tamarins, Saguinus oedipus held in captivity and given the opportunity of assisted learning can complete tool-related tasks however speculation exists surrounding their actual understanding of the folk physics involved (Hausser, 2002). A kin to the woodpecker finches, the egyptian vultures, the tufted capuchins, Cebus apella and the chimpanzee, Pan troglodytes these animals most likely utilize the trial and error approach to develop positive associations for the correct actions required to obtain their reward (Povinelli (chimpanzees), 2000; Hauser (chimpanzees), 1997; Fujita (tufted capuchins), 2003; Evans &amp; Westergaard (tufted capuchins), 2004). All these species are generally considered to analyse and perform their actions based on associative learning (Povinelli et al, 2000).

Rook
One rook (Corvus frugilegus) out of seven tested were shown to complete transfer tasks however it was thought that the rook used a rule abstration technique rather than causal reasoning and the inconsistency across the seven rooks performance makes them subdominant to the NC crow (Seed et al, 2006). They can however solve a modified trap-tube quicker than chimpanzees (Seed et al, 2006).

= Introducing the NC Crow as a model system =

In science we are always interested in discovering new model systems which can be used to gain insight into the physiology of our own body’s. Finding models for Neuroscience research presents a greater challenge compared with other fields due to the disproportionate cognitive evolution we have undertaken and the obvious fact that the majority of animals do not share our cognitive abilities and hence these neural circuitries are not avilable for study. This then obviates the importance of finding animals with enhanced cognitive capabilities previously thought to be possessed only by humans. In this next section I will be demonstrating how the NC crow may contribute as a model system in the study of:


 * Lateralization of the brain
 * The evolution of problem solving
 * The mechanism of behavioural trait transmission
 * The evolution of tehnology
 * Analogical Reasoning
 * The use of folk physics to solve tasks

A model for lateralization
There is a strong population bias for right handedness in the human population and understanding why this is will provide insight into how our brains have evolved and further characterize the lateralization of our brain. Two strong theories for the selective pressure of lateralization include: the first postulates that the development of language and speech processing resulted in the consequential specialization of the left hemisphere (Deacon, 1997), and; the increased specialization of the left hemisphere resulted from the need for increased brain organization following the development of manipulatory skills including tool making (Ward and Cantalupo, 1997). Solving this problem will lend evidence to elucidate the earliest common ancestor of humans through which specialization began, i.e. the growing evidence suggesting that there is lateralization among non-humans supports the idea that hemispheric specialization occurred anciently and was present in the four-limbed common ancestor of birds and mammals (Rogers, 1989; Bradshaw, 1991; Bisazza et al, 1998) or the opposing view which portrays hemispheric specialization occurring during the common ancestor of monkeys and humans following the selection of handedness (MacNeilage et al, 1987). With this in mind I propose that the NC crow would make an excellent model for strengthening one of the views surrounding this argument. Since it is a proficient non-human tool user analyzing the handedness of these creatures and studying their neuroanatomy will elucidate what factors cause brain lateralization. The tapered leaf tools can be cut from the left or right edge of the pandanus leaves. Hunt (2000b) proposed that the cuts made on pandanus leaves were bias at a local population level for cutting along the left edge of the leaf whilst there appeared to be no physical factors conferring this dominance and hence he concluded that it must be due to functional lateralization. This study was later extrapolated to include the entire island of New Caledonia using a large sample size of 3,727 stepped-cut counterparts (the gap missing in a pandanus leaf following removal of leaf tool) and the result was the same (Hunt et al 2001). This observation is consistent with Rogers (1996) and Gunturkun (1997) who found specialization of the right eye in object related tasks in chickens and in pidgeons. These results suggest the causation for lateralization is to increase the efficiency of complex sequential processing communication within the brain (Hunt et al 2001). A detailed anatomical analysis and diligent experimentation of their brains will investigate this phenomenon. The factors affecting the strength of functional specialization between hemispheres are not well known although it is thought that more complex tasks demonstrating handedness reflect a population level cerebral specialization and therefore it is reasonable to predict a positive correlation between the complexity of the manipulatory task and the strength of handedness within the population (Healey et al, 1996; Fagot &amp; Vauclair, 1991). The NC crow’s tool use activities may serve as a fantastic model for defining the technological evolution of humans as the manipulatory complexity of tool manufacture is considered to be greater than the tools subsequent use (Rutledge &amp; Hunt, 2004) and therefore the neural mechanisms conducting both behaviours may be individually lateralized (McGrew &amp; Marchant, 1999; Hunt et al, 2001; Rutledge &amp; Hunt, 2004; Lonsdorf &amp; Hopkins, 2005). Another reason that the NC crows are a good model for analysing population-level laterality is the fact that their tool manufacturing is achieved through a single bill which allows control of the confounding effects associated with using two independent limbs (Hunt et al, 2006). An important distinction between the analysed tool use between the non-human primates and the NC crows is that the crows do not exhibit any ambilaterality which is demonstrated with primates (McGrew &amp; Marchant, 1997; Lonsdorf &amp; Hopkins, 2005). Since the complexity of the NC crows tool use tasks are greater than the more primitive tasks of the primates it follows logically that the more complex tasks would require more lateralisation. These birds therefore may provide the link between non lateralized brain activities, those partially lateralized and tasks exhibiting full lateralization. Because the crows manufacture three distinctly different designs from the pandanus tree with varying complexity in both manufacture and use (with the stepped cuts involving the greatest manipulation and the. This provides an even finer comparable scale then comparing between species as we can analyse the differences in laterality within the species between closely related tasks with only subtle differences in manipulatory complexity. Hunt et al 2006 demonstrated for the first time evidence for the assumed link between design complexity and laterality using the outline of pandanus leaf cut-outs, called counterparts, in which the handedness of the operation could be easily noted based on which edge of the leaf was used. Lonsdorf &amp; Hopkins (2005) found a population-level handedness in non human primates which would suggest that tool use may have not played a big role in the early evolution of laterality in humans however may provide speculator insight into what factors drove the intense handedness witnessed in our race. In fact the opposing theory of language being the instigator of handedness may be a consequence of tool use depending on whether communication and coordination between human individuals preceded tool use or resulted from it. Whilst Hunt et al (2006) discovered a positive correlation between tool manufacture complexity and laterality no such correlation was found for the actual use of the manufactured tools. This likely reflects the neural pathways involved in the two tasks with the tool-use pathways demonstrating more cerebral symmetry than the manufacturing pathways. The NC crow therefore may also serve as a model organism for anatomically and functionally distinguishing the boundaries of these pathways. Findings of handedness in chimpanzees (McGrew &amp; Marchant, 2001) has only been achieved for animals in captivity and evidence for wild free-living examples of population-level handedness is lacking and required to rule out the possibility that it is human influence conferring this phenomenon.

Spontaneous Meta-tools use &amp; Analogical Reasoning.
Meta-tool use has been postulated as the source of our cognitive leap (de Beaune, 2004). The main cognitive requirement of meta tools use is the ability to hierarchaly organize a sequence of steps each solving a subgoal to summate to the overall goal. Successful completion of a meta tool task in a study by Taylor et al (2007) involved the NC crows using a small stick to obtain a larger stick which subsequently allowed for the extraction of food from a hole. All of the seven crows developed the ability to successfully complete the task whilst 3 of them completed it on their first trial. In contrast; Gorrillas, chimpanzees, capuchin monkeys and Japanese macques showed a far weaker performance in this task with none of the group having all their members developing meta-tool use. It was thought due to the nature of the way the NC crows solved the meta-tool task that they were not solving the task through trial and error resulting from random probing since the correct sequence requiring food extraction was followed very consistently and the tool box containing a useless stone was only very rarely probed. One possibility for the crows performance in this task is that they have the ability to use analogical reasoning in which solving the task followed the construction of an analogy matching their experience in previous problems to the structurally similar novel task. Analogical reasoning may be the discerning factor between exceptional tool-users like the NC crow and those weaker performers such as the great apes.

Using Folk Physics
Many animals have been demonstrated to utilize some form of tool however it is thought that animals lack an understanding of physical forces and causal relations between forces (Weir et al, 2002). Hunt (2000a) observed NC crows in the wild and found that the twigs selected for tool use shared the common characteristics of being older, drier and less flexible than the fresher more flexible non selected twigs. Furthermore he noticed that the birds were far more likely to retrieve a tool following analysis of the hole, which would imply that a tool was selected to suit the task and tool selection is not random. In the course of extracting larvae from a hole crows will commonly discard a less suitable tool for one more ideal for the task, as witnessed by Hunt (1996) and Le Goupils (1928), demonstrating their ability to differentiate between a tools properties and a tasks requirements. The stepped-cut tools made from pandanus leaves are good evidence that they are aware of their intentions before they begin the manufacturing process. Hunt (2000b) reported that the crows must be replicating specific predetermined tool forms due to the consistency of the resulting shapes, the one-step manufacturing process which only rarely involved fine tuning of the design following removal from the plant. The information for the tools design is hypothesized to be stored in the neural circuitries of their brains since crows do not need templates or other birds to mimic their activity. The NC crow also deserves particular mention of their ability to spontaneously solve novel problems (Taylor et al, 2007). Wild NC crows make at least two distinctive types of hooks using specific techniques however in the synthetic environment the bending of pliable materials including wires has been demonstrated involving novel technique otherwise unreported in the wild and likely to be ineffective in a natural habitat suggesting a novel thought process and problem solving ability (Weir et al, 2002). Experimentally the ability to purposefully manipulate objects for use as tools without extensive prior teachings, observation of bending and ability to observe and imitate the process are very rare even in non-human primates (Weir et al, 2002). Hunt et al (2000a. demonstrated that tool use was not a crows first call to action, rather the consequence of the depth of the larvae requiring a tool to extract it. During the manufacture of hooked twig tools NC crows, according to Hunt &amp; Gray (2004a), always chose forked twigs specifically as the material to make their tools with. Their method of pulling the side twigs from the future tool was always non-random and eventuated in a hook being formed following snipping of the side twig at the base rather than pulling it off (which would be physically easier but not produce a hook at the twig forks). The routine nature of their actions involved in making hooked tool is definitely indicative of the crows understanding of their intended goal and the fact that no trial and error is required to find the functional working end of the tool would suggest that an understanding of the functional domains within the tool are understood. Weir et als (2002) held captive a crow, Betty, which quickly learnt how to bend wires to make tools. In contrast to chimpanzees who have never been shown to do this evidence may suggest NC crows have somewhat a rudimentary understanding of the general folk physics and properties with which the materials of this world abide by (Hunt &amp; Gray, 2004a). An important finding in this study was that the task was able to be completed without a trial and error approach as the material was unfamiliar to the crow but however did not imede its ability to modify the material with as much ease as the learned materials. Two crows, Abel (male) and Betty (female), held in captivity and analysed by psychologist Alex Kacelnik reportedly selected the appropriate legnth of stick to be used in a stick tool epxeriment where the legnth of the tool closely matched the distance between the food and the hole (Chappel and Kacelnik, 2002). Furthermore the diameter of the stick tool was undestood by Betty as she would select the idal thickness to fit through the holes in the food barricade (Chapell &amp; Kacelnik, 2004).

Associative vs causal reasoning
Associative learning is the linking of two events and assigning a basic ‘good’ or ‘bad’ association with the linkage. Causal understanding or learning involves matching a reason to the linkage, a ‘how’ or ‘why’ paradigm. Causal understanding leads to prediction and inference whilst associative learning only leads to repition of successful events. Assigning causal reasoning to an animals intellect has thus far been problematic, controversial and disputed among a variety of species. Associative learning may only be implemented should a novel task provide perceptual similarities to a previously completed task. Causal reasoning however provides the subject with the ability to apply previously larnt concepts to a novel task in the absence of perceptual familiarities. In a commonly used psychological test called the trap-tube test animals may be analysed to assess whether they utilize causal reasoning to solve a physical problem. The test allows the animal to obtain a food reward should they use the correct direction to release the food fom the tube, hence avoiding a trap. The tube contains two visibly identical holes except that one is barricaded by a supporting structure and hence moving the food out the side containing the hole will result in the food being trapped. Gravity acts as the causal mechanism conferring the loss of food rewards that are unsupported by the tubes structures. Tufted capuchins and chimpanzees showed no ability to learn the concept of avoiding the trap tube when the location of the trap was changed leading scientists to assume that these species use associative cues for their learning rather than causal reasoning (Visalberghi &amp; Limongelli, 1994; Povinelli, 2000). These species probably link the food reward with the direction they had to push the food out rather than depicting the trap tube as being the facet of the task that is important. The trap tube task however may be flawed in its ability to definitvely assign this distinction to animals. (needs more elabouration) In a similar experiment, the trap table, an animal subject is given the opportunity to rake a food reward using a tool during which the food is either successfully pulled along the flat surface or falls into the hole (Taylor et al, 2008). The causal features being tested are the concepts that objects may not move through other (solid) objects, objects move successfully along flat surfaces and gravity pulls objects downwards into regions where the food may not be obtained(Taylor et al, 2008). Again this test for causal reasoning is flawed as we can assume an animal has used causal reasoning to solve the task. For instance the sight of the hole may be producing a negative association with that side of the trap table causing the animal to chose the other sid without ever having any actual understanding of gravity’s effect on the unsupported food rewards(Taylor et al, 2008). The animals may have already basic associations in place to avoid holes in general as they are generally problematic. A more complete method to assess causal understanding called transfer triangulation acts to rmeove the associative aspects confounding the causal study (Heyes, 1993). A series of tasks requiring the same causal inferences whilst containing distinctly different associaitvie cues are constructed and a subjects ability to transfer their causal understanding between tasks without having to learn new associative event pairs. A simple combination fo trap tube and trap table tasks will produce this triangulative series. In a study by Martin-Ordas et al (2008) 20 individuals accros 4 ape species were shown to successfully learn one of the task but all of them failed to tranfer their knowledge between tasks. Transfer triangulation whilst being more robust than the two tasks independently still has its flaws(Taylor et al, 2008). Causal reasoning may be utilized by individuals producing a failed result however each causal concept may be linked to a specific action and transfer of causal reasoning between acions may be lacking(Taylor et al, 2008). Associative learning may also still be the major, if not only, influence affecting the successful completion of the task as a link between flat surfaces and food reward may be generated (Taylor et al, 2008). If the New Caledonian crow uses cognitive causal reasoning suggested to be on the frontier of non-human performance than we would expect the crows to perform well in each of the tasks and transfer studies. Taylor et al (2008) set out to assess this hypothesis. These used the rudimentary trap tube intially and then following successful completion the crows were given four transfer tasks each aimed at removing one of the possible arbitrary associative clues, namely the blue rim on the trap hole, the opaque yellow discs at the top and bottom of the tubes and the colour of the disc (being changed to black) and finally they were presented with the trap table task containing none of these arbitrary clues in the hope of removing the concept of using multiple independent cues. Success in each following transfer task should rule out the possibility that the clues associated with each previous task were not used and hence suggesting a causal approach. Transfer task 3 involved having two holes with one blocked with an orange opaque disc, success required the movement of the food into the empty hole. Failure in transfer three would suggest a causal sensitivity to the hole and success would imply the use of associative learning against the low disc or blue rim. Of the six crows tested three were able to complete the initial tube task. The successful completion of the intial tube task, tranfer tasks 1&amp;2, failure of transfer 3 and success in the trap table task provides good evidence that the crows are causally sensitive to the hole, the impedence of its surrounding structure and gravity’s affect on placing the food within the unobtainable region. These results contrast the chimpanzees performance during Martin-Ordas et als (2008) transfer tasks. The simplistic explanations of chance, generalistic associative visual and tactile cues or prior dispositions were fairly rules out in their experiment. Although far from concrete evidence their study provides the strongest evidence for a non-human using causal reasoning to solve tasks (Taylor et al, 2008). The transfer to the table task also provides evidence for analogical reasoning and it is the combination of analogical reasoning and an understanding of the causal relationships between folk physical attributes that provide the NC crow with their enhanced tool-using capabilities.

The evolution of problem solving
Many thought techniques can be proposed when attempting to psychological profile an animal. Trial and error reasoning involves the production of semi-random success and fail events which may eventuate in the solution and does not create consistent outcomes during the learning of the task. The reason for believing that the NC crow does not employ this technique lies in their consistency at solving novel problems suggesing an inherent understanding of the task and abiity to predict the actions required to solve the task (need reference). Immediate causal inference, more commonyl called insight requires the ability to assess a problem prior to solving it thereby inreasing the consistency to which the problem is sovled. In an experiment by Hunt et al (2006) in which non-natural wooden holes were developed containing cerambycida larva at the bottom the NC crow was unable to predict the holes depth demonstrated by the lack of correlation between the hole depth and primary stick legnth selection. This could possibly be the result of a lack of depth perception and not necessarily a lack of understanding of the relationship between stick legnth and hole depth but in either way the results do not support the idea that they use immediate causal inference to solve this particular problem. A two-stage heuristic strategy involves implementing a previously defined strategy (obtained through trial and error) which typically solves closely related problems prior to adjusting the behaviour in a fine-tuning manner using trial and error should the default solution be unsuccessful. Following failure of the default routine a trial and error approach may not be initialized however and a simple rule strategy may be applied for example: Failing to fit a stick tool through a smaller diameter gap may induce the action of selecting a thinner stick tool and this action is repeated until the stick will penetrate the hole regardless of the animals understanding of importance of the relationship between the stick and holes diamter and the concept of the two needing to match. This theory fits the NC crows intellect the best since a trial and error approach can be ruled out due to the fact that the selection of the secondary stick was not random and did not produce mean legnths which surround the primary stick legnth being both longer and shorter (Hunt et al, 2006). Conversly, and in accordance with the theory, the legnth of the second stick were on average longer than the primary one selected. This theory is further supported by Weir &amp; Kacelnik’s (2006) experiment during which Betty in the majority of trials initially used the unbent wire to attempt to obtain a small bucket of food from a tube. Despite this method having a 90% fail rate this attempt was repeated sugesting it was the default behaivour and only modified following failure. This two-stage heuristic strategy proposed to be employed by the NC crows is in contrast to the non-human primates who require considerable training in order to obatin consistent success in similar tool-problems (Povinelli, 2000).

Cultural versus genetic transmission
How the NC crows obtained their tool behavior is unknown. It is thought that the early ancestors of human obtained their tool-making skills socially (Isac, 1976; Tattersall, 1998). The inheritance of tool use characteristics may serve as a very suitable model for either the transmission of intelligence through either cultural or genetic transmission. NC crows have been observed (Hunt, 2000a) using tools to gather prey in the presence of their juveniles with special mention made of their close attention paid by the juveniles and attempts made to replicate the parents actions following the ‘training’. It is clear that juveniles are less experienced and skilful at their feeding tasks meaning that their skills are learned and the process by which this occurs may provide insight into the mechanisms of cognitive learning and memory processing and the cultural transmission of technological skills between adult and juveniles in nonhumans. Hunt (2000a, 1996) demonstrated that, as with Chimpanzees (Boesch &amp; Boesch 1990, McGrew 1992) NC crows in different location demonstrate different tool traditions each having evolved to their specific activities. Understanding how the NC crows obtained their adaptive behaviors may dissect the mechanisms behind humans evolutional leaps. If cultural transmission is deemed to be the route of their education then they might provide a suitable model for the cognitive, behavioral and social processes involved in transmitting the information without the use of language (Dibble, 1989). Crows spend most of their time in families of parents and dependent juveniles in which it is during the first year that the juveniles developstick-tool capabilities (Holzhaider et al, unpublished data). This familial organization promotes the cultural transmission of tool-use techniques. NC Crows are described to have a considerable amount of determination and patience when it comes to working through a feeding task using a tool. Hole probing to retrieve larvae has been observed to commonly carry on for 10minutes before successful removal. Patience and determination is very central to learning and consequentially mental evolution and this may help explain their success as a technologically advanced species.

Convergent Evolution
It would appear that the Corvidae have convergently evolved characteristics which rival those to the primates (Emery &amp; Clayton, 2004). The NC crow being the most proficient at tasks mimicking those which exemplify the primates abilities makes them the prime candidate to study the possibility of convergent evolution and the mechanisms which contributed to their convergence.

= Do they attend to the functional properties of their tools? =

To ascertain whether the functionally relevant features of a tool were understood to be important to the NC crow Holzhaider et al (2007) conducting a series of experiments in which the functional domains of pandanus leaf tools were used to assess this.

Experiment 1: The direction of the barbs confers their appropriate functioning in the pandaus leaf tool. Some tools were placed in the correct orientation to a hole containing the food reward whilst others in the wrong orientation. Reorientating the tool prior to attempting to use it would imply an understnading of the relvancy of the directions of the barbed ends.

Experiment 2: The barbs of the tools were left intact in some tool and stripped from others. A random selection process between the two types would suggest a lack of understnading of the need for the barbs. Sourced from: Holzhaider et al (2007).

Results: Whilst the results between the NC crows tested were often conflicting overall there was insignifcant evidence to suggest they were attending to the functional features of the pandaus leave since there was no difference between the latnecies (time taken to flip the tool) in the barbs-up or barbs-down positions (Holzhaider et al, 2007) as well as there being an insignificant difference between the selection of barbed and barless pandaus tools.

Discussion: The results suggest the possibility that NC crows may use an association learned from the relationship between the procdure and the success of food extraction without understanding what aspects of their actions are contributing to the success.

= Future Studies: =

Much more work is required to elucidate the full cognitive potential of these birds especially involving non-tool cognition. Studying the NC crow may provide powerful experimental platforms to gain insights into the evolution of complex cognition. Coupled with the small sample size of the experiment completed by Kenward et al (2005) and the lack of an ability to quantify the ability to and progress of tutoring further experiments are required to assess the distinction between socially acquired and inherited tool use traits, particularly involving more complex tasks. The elucidation of the degree of cognitive involvement in these complex physical actions is required to understand how cognitively evolved these birds are. Monoocular tests can be performed to assess the comparable anatomy and contributions made by each visual system (left and right) during avian tool use tasks. Analysing the effect that light exposure has during embryonic development on the handedness of the resulting organism may help evaluate the theory that handedness begins as a slight advantage obtained by one hemisphere and is strengthened through experience.

=References=

C.U. Ariëns-Kappers, The ontogenetic development of the corpus striatum in birds and a comparison with mammals and man, Kon Akad v Wetensch te Amsterdam 26 (1920), p. 135.

Ashby FG, Ennis JM, Spiering BJ (2007): A neurobiological theory of automaticity in perceptual categorization. Psychol Rev 114:632–656.

Beck, B.B (1980) Animal tool behaviour: the use and manufacture of tools by animals. New York: Garland Bird (1999) Cooperation and conflict: The behavioural ecology of the sexual division of labour. Evol.Anthropol. 8, 65-75

Boesch, C. &amp; Boesch, H. 1990. Tool use and tool making in wild Chimpanzees. Folia Primatologica 54, 86-89.

Boesch, C (1996) The question of culture, Nature 379, 207-208

Bradshaw, J.L (1991) Animal asymmetry and human heredity: dextrality, tool use and language evolution-10years after Walker (1980). Br. J.Psychol. 82, 39-59

Chappel &amp; Kacelnik (2002) Tool selectivity in a non-primate, the New Caledonian Crow, Animal Cognition 5:71-78. Chappel &amp; Kacelnik (2004) Selection of tool diameter by New Caledonian Crows, Animal Cognition 7:121-127 Cnotka J, Güntürkün O, Gray RD, Rehkämper G, Hunt GR (2008): Extraordinary large brains in tool-using New Caledonian crows (Corvus moneduloides). Neurosci Lett 433:241–245. Deacon, T. (1997) The symbolic species: the co-evolution of language in the human brain. London: Allen Lane The Penguin Press. Dibble, H.L. (1989) The implications of stone tool types for the presence of language during the Lower and Middle Paleolithic. In The human revolution: behavioural and biological perspective on the origin of modern human, pp 415-432. Princeton University Press.

Evans &amp; Westergaard (2004) Discrimination of functionally appropriate and inappropriate throwing tools by tufted capuchins (Cebus apella), Animal Cognition 7:255-262 Fagot, J. &amp; Vauclair, J. 1991 Manual laterality in nonhumanprimates: a distinction between handedness and manual specialization. Psychol. Bull. 109, 76–89. (doi:10.1037/0033-2909.109.1.76) Feenders G, Liedvogel M, Rivas M, Zapka M, Horita H, Hara E, Wada K, Mouritsen K, Jarvis ED (2008): Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLoS One 3:e1768.

Fujita et al (2003) How do tufted capuchin monkeys (Cerbus apella) understand causality involved in tool use? Jounral of Experimental Psychological Animal Behavoural process 29:233-242 Gill, F.B. (1989) Ornithology. New York: W.H.Freeman &amp; Co.

Grafen, A. 1989. The phylogenetic regression. Philosophical Transactions of the Royal Society of London B 326:119-157. de Beaune, S.A. (2004). The invention of technology: prehistory and cognition. Curr. Anthropol. 45, 139–162. O. Güntürkün, Cognitive impairments after lesions of the neostriatum caudolaterale and its thalamic afferents in pigeons: functional similarities to the mammalian prefrontal system?, J. Brain Res. 38 (1997), pp. 133–143. Güntürkün, O. (1997) Avian visual lateralization: a review, Neuroreport 8, iii-xi.

Gu¨ntu¨rku¨n, O., Diekamp, B., Manns, M., Nottelmann, F., Prior,H., Schwarz, A. &amp; Skiba, M. 2000. Asymmetry pays: visual lateralization improves discrimination success in pigeons. Current Biology, 10, 1079e1081. Hausser (1997) Artificial kinds of functional design features: what a primate understands without language, Cognition 64:285-308 Hauser MD, Pearson H, Seelig D (2002) Ontogeny of cotton-top tamarins, Saguinus oedipus: innate recognition of functionally relevant features. Anim Behav 64:299–311

Healey, J. M., Liederman, J. &amp; Geschwind, N. 1986 Handedness is not a unidimensional trait. Cortex 22,33–53.

Heyes, C. M. 1993 Anecdotes, training, trapping, and triangulating: do animals attribute mental states? Anim. Behav. 46, 177–188. (doi:10.1006/anbe.1993.1173)

Holzhaider JC, Hunt GR, Campbell VM, Gray RD (2008): Do wild New Caledonian crows (Corvus moneduloides) attend to the functional properties of their tools? Anim Cogn 11:243–254.

Hume, D. 1739/1978 A treatise on human nature. Oxford, UK: Clarendon Press.

Hunt, G. Manufacture and use of hook-tools by New Caledonian Crows (1996), Nature, 379(18) 249-251. Hunt, G.R. 2000. Human-like, population-level specialisation in the manufacture of pandanus tools by New Caledonian Crows Corvus moneduloides. Proceedings of the Royal Society, London, B.267, 403-413.

Hunt &amp; Gray (2007) Parallel tool industries in New Caledonian crows. Biology Letters, Evol. Bio. University of Auckland.

Hunt, G. R. 1996 Manufacture and use of hook-tools by NewCaledonian crows. Nature 379, 249–251. (doi:10.1038/379249a0) Hunt, G. R. 2000 Human-like, population-level specializationin the manufacture of pandanus tools by New Caledonian crows Corvus moneduloides. Proc. R. Soc. B267, 403–413. (doi:10.1098/rspb.2000.1015) Hunt, G. R. &amp; Gray, R. D. 2003 Diversification and cumulative evolution in New Caledonian crow tool manufacture. Proc. R. Soc. B 270, 867–874. Hunt, G. R. &amp; Gray, R. D. 2004 Direct observations ofpandanus-tool manufacture and use by a New Caledonian crow (Corvus moneduloides). Anim. Cogn. 7, 114–120.(doi:10.1007/s10071-003-0200-0)

Hunt et al (2006) Design complexity and strength of laterality are correlated in New Caledonian crows pandanus tool-manufacture, Proc. Of the Royal Society, Published online 23 Feb 2006, doi:10.1098/rspb.2005.3429 Hunt, G. R., Corballis, M. C. &amp; Gray, R. D. 2001. Laterality in tool manufacture by crows. Nature, 414, 707. Isaac, G.L 1976 Stages of cultural elaboration in the Pleistocene: possible archaeological indicators of the development of language capacilities. Ann. NY Acad. Sci. 280, 275-288

Iwaniuk AN, Dean KM, Nelson JE (2004): A mosaic pattern characterizes the evolution of the avian brain. Proc R Soc B Suppl 271:S148–S151.

Jarvis ED, Mello CV (2000): Molecular mapping of brain areas involved in parrot vocal communication. J Comp Neurol 419:1–31. E.D. Jarvis, O. Güntürkün, L. Bruce, A. Csillag, H.J. Karten, W. Kuenzel, L. Medina, G. Paxinos, D.J. Perkel, T. Shimizu, G. Striedter, M. Wild, G.F. Ball, J. Dugas-Ford, S. Durand, G. Hough, S. Husband, L. Kubikova, D. Lee, C.V. Mello, A. Powers, C. Siang, T.V. Smulders, K. Wada, S.A. White, K. Yamamoto, J. Yu, A. Reiner and A.B. Butler, Avian brains and a new understanding of vertebrate brain evolution, Nat. Rev. Neurosci. 6 (2005), pp. 151–159.

H.J. Karten, The organization of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon, Ann. N.Y. Acad. Sci. 167 (1969), pp. 164–179.

Lefebvre L, Nicolakakis N, Boire D (2002): Tools and brains in birds. Behavior 139:939–973. Le Goupils, M. 1928. Dans la Brousse Calédonienne: Souvenirs d’un Ancien Planteur 1898–1904. Perrin, Paris.

Lieberman, P. (1991) Uniquely Human: The evolution of speech, thought and selfless behaviour. Cambridge, MA: Harvard University Press.

Limongelli, L., Boysen, S. T. &amp; Visalberghi, E. 1995 Comprehension of cause–effect relations in a tool-using task by chimpanzees (Pan troglodytes). J. Comp. Psychol. 109, 18–26. (doi:10.1037/0735-7036.109.1.18)

Lonsdorf, E. V. &amp; Hopkins, W. D. 2005 Wild chimpanzees show population-level handedness for tool use. Proc. NatlAcad. Sci. USA 102, 12 634–12 638. (doi:10.1073/pnas.0505806102)

Marchant, L. F., McGrew,W. C. &amp; Eibl-Eibesfeldt, I. 1995 Ishuman handedness universal? Ethological analyses from three traditional cultures. Ethology 101, 239–258.

Mariotti, J. 1996. Les Contes de Poindi. Grain de Sable, Nouméa. (First published in 1937 in Revue de Paris, pp.351-389.)

Martin-Ordas, G., Call, J. &amp; Colmenares, F. 2008 Tubes, tables and traps: great apes solve two functionally equivalent trap tasks but show no evidence of transfer across tasks. Anim. Cogn. 11, 423–430. (doi:10.1007/s10071-007-0132-1) McGrew, W.C. 1992. Chimpanzee Material Culture: Implications for Human Evolution. Cambridge University Press, Cambridge.

McGrew, W.C. 1992 Tool-use by free ranging chimpanzees: the extent of diversity. J.Zoo228, 689-694 Mellers, P. (1989) Major issues in the emergence of modern humans. Current. Anthropol. 30, 349-385

McGrew, W. C. &amp; Marchant, L. F. 1997 Using the tools athand: manual laterality and elementary technology in Cebus spp. and Pan spp. Int. J. Primatol. 18, 787–810.(doi:10.1023/A:1026347913888) McGrew, W. C. &amp; Marchant, L. F. 2001 Ethological study ofmanual laterality in the chimpanzees of the Mahale mountains, Tanzania. Behaviour 138, 329–358. (doi:10.1163/15685390152032497)

Mellars, P. The Human Revolution (eds. Mellars,P. &amp; Stringer,C.) 338-365 Princeton University Press, New Jersey, 1989. Millikan GC, Bowman RI (1967) Observations on Gal ´ apagos tool-using ﬁnches in captivity. Living Bird 6:23–41

Nagel K, Olguin RS, Tomasello M (1993) Processes of social learning in the tool use of chimpanzees (Pan troglodytes) and human children (Homo sapiens). J Comp Psychol 107:174–186

Nieuwenhuys R, ten Donkelaar, HJ, Nicholson C (1998): The Central Nervous System of Vertebrates. Berlin, Springer. Orenstein, R.I. 1972. Tool-use by the New Caledonian Crow (Corvus moneduloides). Auk 89, 674-676.

Portmann A, Etudes sur la cérébralisation chez les oiseaux. II. Les indices intracérébraux, Alauda 15 (1947), pp. 1–15.

Povinelli DJ (2000) Folk physics for apes: the chimpanzee’s theory of how the world works. Oxford University Press, Oxford

G. Rehkämper and K. Zilles, Parallel evolution in mammalian and avian brains: comparative cytoarchitectonic and cytochemical analysis, Cell. Tissue Res. 263 (1991), pp. 3–28.

Reid, J.B (1982) Tool-use by a rook, and its causation. Anim. Behav. 30, 1212-1216 Rogers, L.J. (1989) Laterality in animals. Int. J.Comp.Psychol. 3,5-25

Rutledge, R. &amp; Hunt, G. R. 2004 Lateralized tool use in wildNew Caledonian crows. Anim. Behav. 67, 327–332.(doi:10.1016/j.anbehav.2003.07.002)

Seger CA (2008): How do the basal ganglia contribute to categorization? Their role in generalization, response selection, and learning via feedback. Neurosci Biobehav Res 32:265–278. Tattersall, I. (1998) Becoming human: Evolution and human uniqueness. Orlando, FL: Harcourt Brace&amp;Co.

A.H. Taylor, G.R. Hunt, J.C. Holzhaider and R.D. Gray, Spontaneous metatool use by New Caledonian crows, Curr. Biol. 17 (2007), pp. 1504–1507

Tebbich S, Bshary R (2004) Cognitive abilities related to tool use in the woodpecker ﬁnch, Cactospiza pallida. Anim Behav 67:689–697 Thouless CR, Fanshawe JH, Bertram CR (1987) Egyptian vultures Neophron percnopterus and Ostrich Struthio camelus eggs: the origins of stone-throwing behaviour. Ibis 131:9–15

Timmermanns S, Lefebvre L, Boire D, Basu P (2000): Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain Behav Evol 56:196–203.

Visalberghi, E. &amp; Limongelli, L. 1994 Lack of comprehension of cause–effect relations in tool-using capuchin monkeys (Cebus apella). J. Comp. Psychol. 108, 15–22. (doi:10.1037/0735-7036.108.1.15)

A.A.S. Weir, J. Chappell and A. Kacelnik, Shaping of hooks in New Caledonian crows, Science 297 (2002), p. 981 A.A.S. Weir and A. Kacelnik, A New Caledonian crow (Corvus moneduloides) creatively re-designs tools by bending or unbending aluminium strips, Anim. Cogn. 9 (2006), pp. 317–334.

Weir, A. A. S., Kenward, B., Chappell, J. &amp; Kacelnik, A. 2004 Lateralization of tool use in New Caledonian crows(Corvus moneduloides). Proc. R. Soc. B 271, S344–S346.(doi:10.1098/rspb.2004.2803)

Weir AAS, Kacelnik A (2006) New Caledonian crows (Corvus moneduloides) creatively re-design tools by bending or unbending metal strips according to needs. Anim Cogn DOI: 10.1007/s10071-0060052-5 Weir AAS, Chappell J, Kacelnik A (2002) Shaping of hooks in NewCaledonian crows. Science 297:981 Wickens JR, Horvitz JC, Costa RM, Killcross S (2007): Dopaminergic mechanism in actions and habits. J Neurosci 27:8181–8183.