‘Captivity bias’ in animal tool use and its implications for the evolution of hominin technology

Animals in captive or laboratory settings may outperform wild animals of the same species in both frequency and diversity of tool use, a phenomenon here termed ‘captivity bias’. Although speculative at this stage, a logical conclusion from this concept is that animals whose tool-use behaviour is observed solely under natural conditions may be judged cognitively or physically inferior than if they had also been tested or observed under controlled captive conditions. In turn, this situation creates a potential problem for studies of the behaviour of extinct members of the human family tree—the hominins—as hominin cognitive abilities are often judged on material evidence of tool-use behaviour left in the archaeological record. In this review, potential factors contributing to captivity bias in primates (including increased contact between individuals engaged in tool use, guidance or shaping of tool-use behaviour by other tool-users and increased free time and energy) are identified and assessed for their possible effects on the behaviour of the Late Pleistocene hominin Homo floresiensis. The captivity bias concept provides one way to uncouple hominin tool use from cognition, by considering hominins as subject to the same adaptive influences as other tool-using animals.     

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

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

动物使用工具行为研究进展北大核心CSCD

使用工具曾被认为是人类独有的能力,然而,在过去的50年中,学界逐渐认识到工具的使用普遍存在于整个动物界。其中,使用工具最多的类群是哺乳类、鸟类和昆虫。动物使用工具有一定目标性,然而大多数动物仅考虑当前的目标,而非长远目标。动物使用工具的行为受到环境因素和动物自身认知能力、生理特点与进化历史的影响,并可能表现出一定的个体差异。有些动物使用工具的行为是与生俱来的,然而大部分高等动物通过试错学习获得使用工具的能力。通过模仿学习,一些使用工具的行为可以传播和演化,从而在种群中广泛分布。工具的使用是动物认知领域的核心概念之一,开展动物使用工具的研究,能够加深对动物认知能力和行为进化的理解。     

The study of tool use as the way for general estimation of cognitive abilities in animals

Investigation of tool use is an effective way to determine cognitive abilities of animals. This approach raises hypotheses, which delineate limits of animal's competence in understanding of objects properties and interrelations and the influence of individual and social experience on their behaviour. On the basis of brief review of different models of manipulation with objects and tools manufacturing (detaching, subtracting and reshaping) by various animals (from elephants to ants) in natural conditions the experimental data concerning tool usage was considered. Tool behaviour of anumals could be observed rarely and its distribution among different taxons is rather odd. Recent studies have revealed that some species (for instance, bonobos and tamarins) which didn't manipulate tools in wild life appears to be an advanced tool users and even manufacturers in laboratory. Experimental studies of animals tool use include investigation of their ability to use objects physical properties, to categorize objects involved in tool activity by its functional properties, to take forces affecting objects into account, as well as their capacity of planning their actions. The crucial question is whether animals can abstract general principles of relations between objects regardless of the exact circumstances, or they develop specific associations between concerete things and situations. Effectiveness of laboratory methods is estimated in the review basing on comparative studies of tool behaviour, such as "support problem", "stick problem", "tube- and tube-trap problem", and "reserve tube problem". Levels of social learning, the role of imprinting, and species-specific predisposition to formation of specific domains are discussed. Experimental investigation of tool use allows estimation of the individuals' intelligence in populations. A hypothesis suggesting that strong predisposition to formation of specific associations can serve as a driving force and at the same time as obstacle to animals' activity is discussed. In several "technically gifted" species (such as woodpecker finches, New Caledonian crows, and chimpanzees) tool use seems to be guided by a rapid process of trial and error learning. Individuals that are predisposed to learn specific connections do this too quickly and thus become enslaved by stereotypic solutions of raising problems.     

Young children spontaneously invent wild great apes’ tool-use behaviours

The variety and complexity of human-made tools are unique in the animal kingdom. Research investigating why human tool use is special has focused on the role of social learning: while non-human great apes acquire tool-use behaviours mostly by individual (re-)inventions, modern humans use imitation and teaching to accumulate innovations over time. However, little is known about tool-use behaviours that humans can invent individually, i.e. without cultural knowledge. We presented 2- to 3.5-year-old children with 12 problem-solving tasks based on tool-use behaviours shown by great apes. Spontaneous tool use was observed in 11 tasks. Additionally, tasks which occurred more frequently in wild great apes were also solved more frequently by human children. Our results demonstrate great similarity in the spontaneous tool-use abilities of human children and great apes, indicating that the physical cognition underlying tool use shows large overlaps across the great ape species. This suggests that humans are neither born with special physical cognition skills, nor that these skills have degraded due to our species’ long reliance of social learning in the tool-use domain.     

Wild‐caught great tits Parus major fail to use tools in a laboratory experiment,despite facilitation

Studies investigating tool use in animals that are not known tool users in the wild are important in helping to understand how and under what circumstances this ability might arise. Tool use appears to be uncommon in great tits (Parus major), with only a single documented observation in which a wild great tit used conifer needles to extract larvae from crevices in trees. In a laboratory‐based experiment, we examined whether wild‐caught great tits could learn to use tools in a similar manner. We presented the birds with two different tool use tasks in which they would need to use either a stick or a hook to extract an otherwise inaccessible meal worm from a transparent plastic tube. First, the birds passed a simpler training criterion (pulling a tool with an attached food reward) that aimed to reduce the difficulty of the task. Nevertheless, none of the individuals learnt to use tools in either of the two tasks. This result stands in stark contrast to the abilities of some corvids and parrots, which can learn to use tools in captivity, even though some of them are not tool users in the wild. We believe that tool use might be difficult for some birds to learn since the skills required for this ability seem not to be part of their natural foraging behaviour.     

Individual and social learning processes involved in the acquisition and generalization of tool use in macaques

Macaques can efficiently use several tools, but their capacity to discriminate the relevant physical features of a tool and the social factors contributing to their acquisition are still poorly explored. In a series of studies, we investigated macaques' ability to generalize the use of a stick as a tool to new objects having different physical features (study 1), or to new contexts, requiring them to adapt the previously learned motor strategy (study 2). We then assessed whether the observation of a skilled model might facilitate tool-use learning by naive observer monkeys (study 3). Results of study 1 and study 2 showed that monkeys trained to use a tool generalize this ability to tools of different shape and length, and learn to adapt their motor strategy to a new task. Study 3 demonstrated that observing a skilled model increases the observers' manipulations of a stick, thus facilitating the individual discovery of the relevant properties of this object as a tool. These findings support the view that in macaques, the motor system can be modified through tool use and that it has a limited capacity to adjust the learnt motor skills to a new context. Social factors, although important to facilitate the interaction with tools, are not crucial for tool-use learning.     

Tool use in wild orang-utans modifies sound production: a functionally deceptive innovation?

Culture has long been assumed to be uniquely human but recent studies, in particular on great apes, have suggested that cultures also occur in non-human primates. The most apparent cultural behaviours in great apes involve tools in the subsistence context where they are clearly functional to obtain valued food. On the other hand, tool-use to modify acoustic communication has been reported only once and its function has not been investigated. Thus, the question whether this is an adaptive behaviour remains open, even though evidence indicates that it is socially transmitted (i.e. cultural). Here we report on wild orang-utans using tools to modulate the maximum frequency of one of their sounds, the kiss squeak, emitted in distress. In this variant, orang-utans strip leaves off a twig and hold them to their mouth while producing a kiss squeak. Using leaves as a tool lowers the frequency of the call compared to a kiss squeak without leaves or with only a hand to the mouth. If the lowering of the maximum frequency functions in orang-utans as it does in other animals, two predictions follow: (i) kiss squeak frequency is related to body size and (ii) the use of leaves will occur in situations of most acute danger. Supporting these predictions, kiss squeaks without tools decreased with body size and kiss squeaks with leaves were only emitted by highly distressed individuals. Moreover, we found indications that the calls were under volitional control. This finding is significant for at least two reasons. First, although few animal species are known to deceptively lower the maximum frequency of their calls to exaggerate their perceived size to the listener (e.g. vocal tract elongation in male deer) it has never been reported that animals may use tools to achieve this, or that they are primates. Second, it shows that the orang-utan culture extends into the communicative domain, thus challenging the traditional assumption that primate calling behaviour is overall purely emotional.     

Tool use by wild cebus monkeys at Santa Rosa National Park,Costa Rica

Although wild cebus monkeys have been observed to use tools, this behavior has been reported only rarely. No one has systematically examined tool use in wildCebus, and it is not known how prevalent tool use is in the species' natural repertoire. During 300 hr of observation on 21 wild capuchins (Cebus capucinus imitator) at Santa Rosa National Park in Costa Rica, 31 incidents of tool use, including eight different types of tool-use behavior, were observed. These observations indicate that tool use is a notable behavior pattern in this troop. Considering these incidents of tool use in conjunction with other reports on complex food-getting and preparation behavior byCebus suggests that tool use is a manifestation ofCebus' high behavioral adaptability. Since onlyCebus and the great apes (especially chimpanzees) have been observed to show such a diverse tool-use repertoire, to use tools so frequently, or to show such complex food-getting behavior in the wild, these observations also support the notion thatCebus and the great apes have followed a parallel evolutionary development of tool-using capacity.     

Sex differences in the stone tool-use behavior of a wild population of burmese long-tailed macaques (Macaca fascicularis aurea)

We investigated sex differences in how Burmese long-tailed macaques (Macaca fascicularis aurea) used stone tools to open shelled food items along the shores of two islands in Laemson National Park, Thailand. Over a 2-week period in December 2009, we collected scan and focal samples on macaques when they were visible along the shores and mangroves. We found females used stones more often while feeding and used smaller tools than males. Females also processed sessile oysters more than males, whereas males processed unattached foods more than females. It was unclear which sex was overall more proficient at stone tool use, but males did perform significantly better at opening unattached food items with large pounding stones. Females also struck food items more times during tool-use bouts and at a faster rate, but no significant difference was found in average tool-use bout duration. Males processed foods slightly faster within a tool-use bout, but we were unable to detect a significant difference in the rate of food processing while foraging with tools. In summary females chipped open sessile oysters with an axing technique more than males, while males used larger stones to pound open unattached shelled food more often than females. Despite using pounding more than females, males also regularly utilized the axing technique on sessile oysters. Our results are the first assessment of sex differences in macaque stone tool use, providing a basis for comparison with tool use in other primates, and to nonfunctional forms of stone use in other macaques.     

Object affordances tune observers' prior expectations about tool-use behaviors

Learning about the function and use of tools through observation requires the ability to exploit one's own knowledge derived from past experience. It also depends on the detection of low-level local cues that are rooted in the tool's perceptual properties. Best known as 'affordances', these cues generate biomechanical priors that constrain the number of possible motor acts that are likely to be performed on tools. The contribution of these biomechanical priors to the learning of tool-use behaviors is well supported. However, it is not yet clear if, and how, affordances interact with higher-order expectations that are generated from past experience--i.e. probabilistic exposure--to enable observational learning of tool use. To address this question we designed an action observation task in which participants were required to infer, under various conditions of visual uncertainty, the intentions of a demonstrator performing tool-use behaviors. Both the probability of observing the demonstrator achieving a particular tool function and the biomechanical optimality of the observed movement were varied. We demonstrate that biomechanical priors modulate the extent to which participants' predictions are influenced by probabilistically-induced prior expectations. Biomechanical and probabilistic priors have a cumulative effect when they 'converge' (in the case of a probabilistic bias assigned to optimal behaviors), or a mutually inhibitory effect when they actively 'diverge' (in the case of probabilistic bias assigned to suboptimal behaviors).     

Do woodpecker finches acquire tool-use by social learning?

Tool-use is widespread among animals, but except in primates the development of this behaviour is poorly known. Here, we report on the first experimental study to our knowledge of the mechanisms underlying the acquisition of tool-use in a bird species. The woodpecker finch Cactospiza pallida, endemic to the Galápagos Islands, is a famous textbook example of tool-use in animals. This species uses modified twigs or cactus spines to pry arthropods out of tree holes. Using nestlings and adult birds from the field, we tested experimentally whether woodpecker finches learn tool-use socially. We show that social learning is not essential for the development of tool-use: all juveniles developed tool-use regardless of whether or not they had a tool-using model. However, we found that not all adult woodpecker finches used tools in our experiments. These non-tool-using individuals also did not learn this task by observing tool-using conspecifics. Our results suggest that tool-use behaviour depends on a very specific learning disposition that involves trial-and-error learning during a sensitive phase early in ontogeny.     

If at first you don't succeed… Studies of ontogeny shed light on the cognitive demands of habitual tool use

Many species use tools, but the mechanisms underpinning the behaviour differ between species and even among individuals within species, depending on the variants performed. When considering tool use ‘as adaptation’, an important first step is to understand the contribution made by fixed phenotypes as compared to flexible mechanisms, for instance learning. Social learning of tool use is sometimes inferred based on variation between populations of the same species but this approach is questionable. Specifically, alternative explanations cannot be ruled out because population differences are also driven by genetic and/or environmental factors. To better understand the mechanisms underlying routine but non-universal (i.e. habitual) tool use, we suggest focusing on the ontogeny of tool use and individual variation within populations. For example, if tool-using competence emerges late during ontogeny and improves with practice or varies with exposure to social cues, then a role for learning can be inferred. Experimental studies help identify the cognitive and developmental mechanisms used when tools are used to solve problems. The mechanisms underlying the route to tool-use acquisition have important consequences for our understanding of the accumulation in technological skill complexity over the life course of an individual, across generations and over evolutionary time.     

Sex differences in young children’s use of tools in a problem-solving task

Three-year-old children were observed in two free-play sessions and participated in a toy-retrieval task, in which only one of six tools could be used to retrieve an out-of-reach toy. Boys engaged in more object-oriented play than girls and were more likely to use tools to retrieve the toy during the baseline tool-use task. All children who did not retrieve the toy during the baseline trials did so after being given a hint, and performance on a transfer-of-training tool-use task approached ceiling levels. This suggests that the sex difference in tool use observed during the baseline phase does not reflect a difference in competency, but rather a sex difference in motivation to interact with objects. Amount of time boys, but not girls, spent in object-oriented play during the free-play sessions predicted performance on the tool-use task. The findings are interpreted in terms of evolutionary theory, consistent with the idea that boys’ and girls’ play styles evolved to prepare them for adult life in traditional environments.     

Gnotobiotically grown aquatic animals: opportunities to investigate host-microbe interactions

The culture of aquatic organisms is still hampered by the occurrence of unpredictable diseases in their early life stages, which are responsible for massive mortalities and considerable economic losses. A better understanding of the host-microbe interactions is certainly essential to develop effective solutions of disease control for the aquaculture industry. As demonstrated in terrestrial animals, the use of gnotobiotic systems (animals cultured in axenic conditions or with a known microflora) can be an excellent tool to extent the understanding of the mechanisms involved in host-microbe interactions and to evaluate new treatments of disease control. Several aquatic animals were cultured so far in germ-free conditions, such as fish, molluscs, crustaceans, rotifers, echinoderms, cnidarians, turbellarians, ascidians and echiurans. The aim of the present review is to recapitulate the findings obtained with gnotobiotic aquatic animals over the last decades, with special emphasis to the host-microbe interactions, as well as the perspectives for future research in this field. In addition, the procedures utilized to culture axenic aquatic animals and to verify contaminations are summarized, and the standardization of these procedures is proposed.     

Setting tool use within the context of animal construction behaviour

Tool use and manufacture are given prominence by their rarity and suggested relation to human lineage. Here, we question the view that tool use is rare because cognitive abilities act as an evolutionary constraint and suggest that tools are actually seldom very useful compared with anatomical adaptations. Furthermore, we argue that focussing on animal tool use primarily in terms of human evolution can lead to important insights regarding the ecological and cognitive abilities of non-human tool users being overlooked. We argue that such oversight can best be avoided by examining tools within the wider context of construction behaviours by animals (such as nest building and trap construction).     

A case of tool use in captive olive baboons (Papio anubis)

Some captive olive baboons can use their tails for picking up objects from the floor. When provided with a short handle and crosspiece, these animals learn to manipulate this tool with their hands, and one of them became proficient in inserting the crosspiece into a small wire loop, attached to a piece of bread and in lifting it up to his cage. Another baboon in the same colony who never used his tail to retrieve objects, did not attempt to use this tool. The psychological aspects of tail-use and tool-use are discussed.     

Tool-use and tool-making by captive, group-living orangutans (Pongo pygmaeus abelii) at an artificial termite mound

The present study examined the use and making of tools to obtain foodstuffs in artificial-mound holes by five captive, group-living Sumatran orangutans (Pongo pygmaeus abelii). Three adult orangutans frequently stripped leaves and twigs from a branch provided (tool-making), and then inserted the tool into a hole to obtain foodstuffs (tool-using). A 5-year-old female juvenile usually used the tools that adult orangutans had previously used, but rarely made tools herself. A 2-year-old male infant did not use any tools. The adult orangutans tend to leave one to several leaves at the top of the branch than to leave many leaves on the branch or to strip all leaves. It seemed likely that tools with appropriate leaves are easier to insert into holes and obtain more foodstuffs, compared with branches with many leaves or sticks without any leaves. When the orangutans were unable to insert a tool into a hole, they usually modified the tool and/or changed their tool-using technique, such as changing how they grasped the tool. These findings are discussed from the perspectives of the orangutan's behavioral flexibility regarding tool-use skills and hierarchical organization in food-processing techniques.     

Tool use, communicative gesture and cerebral asymmetries in the modern human brain

Determining the brain adaptations that underlie complex tool-use skills is an important component in understanding the physiological bases of human material culture. It is argued here that the ways in which humans skilfully use tools and other manipulable artefacts is possible owing to adaptations that integrate sensory-motor and cognitive processes. Data from brain-injured patients and functional neuroimaging studies suggest that the left cerebral hemisphere, particularly the left parietal cortex, of modern humans is specialized for this purpose. This brain area integrates dynamically representations that are computed in a distributed network of regions, several of which are also left-lateralized. Depending on the nature of the task, these may include conceptual knowledge about objects and their functions, the actor's goals and intentions, and interpretations of task demands. The result is the formation of a praxis representation that is appropriate for the prevailing task context. Recent evidence is presented that this network is organized similarly in the right- and left-handed individuals, and participates in the representation of both familiar tool-use skills and communicative gestures. This shared brain mechanism may reflect common origins of the human specializations for complex tool use and language.     

Tool use, aye-ayes, and sensorimotor intelligence

Humans, chimpanzees, capuchins and aye-ayes all display an unusually high degree of encephalization and diverse omnivorous extractive foraging. It has been suggested that the high degree of encephalization in aye-ayes may be the result of their diverse, omnivorous extractive foraging behaviors. In combination with certain forms of tool use, omnivorous extractive foraging has been hypothesized to be linked to higher levels of sensorimotor intelligence (stages 5 or 6). Although free-ranging aye-ayes have not been observed to use tools directly in the context of their extractive foraging activities, they have recently been reported to use lianas as tools in a manner that independently suggests that they may possess stage 5 or 6 sensorimotor intelligence. Although other primate species which display diverse, omnivorous extractive foraging have been tested for sensorimotor intelligence, aye-ayes have not. We report a test of captive aye-ayes' comprehension of tool use in a situation designed to simulate natural conditions. The results support the view that aye-ayes do not achieve stage 6 comprehension of tool use, but rather may use trial-and-error learning to develop tool-use behaviors. Other theories for aye-aye encephalization are considered.