Social influences on delayed gratification in New Caledonian crows and Eurasian jays.

Self-control underlies goal-directed behaviour in humans and other animals. Delayed gratification - a measure of self-control - requires the ability to tolerate delays and/or invest more effort to obtain a reward of higher value over one of lower value, such as food or mates. Social context, in particular, the presence of competitors, may influence delayed gratification. We adapted the 'rotating-tray' paradigm, where subjects need to forgo an immediate, lower-quality (i.e. less preferred) reward for a delayed, higher-quality (i.e. more preferred) one, to test social influences on delayed gratification in two corvid species: New Caledonian crows and Eurasian jays. We compared choices for immediate vs. delayed rewards while alone, in the presence of a competitive conspecific and in the presence of a non-competitive conspecific. We predicted that, given the increased risk of losing a reward with a competitor present, both species would similarly, flexibly alter their choices in the presence of a conspecific compared to when alone. We found that species differed: jays were more likely to select the immediate, less preferred reward than the crows. We also found that jays were more likely to select the immediate, less preferred reward when a competitor or non-competitor was present than when alone, or when a competitor was present compared to a non-competitor, while the crows selected the delayed, highly preferred reward irrespective of social presence. We discuss our findings in relation to species differences in socio-ecological factors related to adult sociality and food-caching (storing). New Caledonian crows are more socially tolerant and moderate cachers, while Eurasian jays are highly territorial and intense cachers that may have evolved under the social context of cache pilfering and cache protection strategies. Therefore, flexibility (or inflexibility) in delay of gratification under different social contexts may relate to the species' social tolerance and related risk of competition.

Socio-ecological correlates of neophobia in corvids.

Behavioral responses to novelty, including fear and subsequent avoidance of novel stimuli, i.e., neophobia, determine how animals interact with their environment. Neophobia aids in navigating risk and impacts on adaptability and survival. There is variation within and between individuals and species; however, lack of large-scale, comparative studies critically limits investigation of the socio-ecological drivers of neophobia. In this study, we tested responses to novel objects and food (alongside familiar food) versus a baseline (familiar food alone) in 10 corvid species (241 subjects) across 10 labs worldwide. There were species differences in the latency to touch familiar food in the novel object and novel food conditions relative to the baseline. Four of seven socio-ecological factors influenced object neophobia: (1) use of urban habitat (versus not), (2) territorial pair versus family group sociality, (3) large versus small maximum flock size, and (4) moderate versus specialized caching (whereas range, hunting live animals, and genus did not), while only maximum flock size influenced food neophobia. We found that, overall, individuals were temporally and contextually repeatable (i.e., consistent) in their novelty responses in all conditions, indicating neophobia is a stable behavioral trait. With this study, we have established a network of corvid researchers, demonstrating potential for further collaboration to explore the evolution of cognition in corvids and other bird species. These novel findings enable us, for the first time in corvids, to identify the socio-ecological correlates of neophobia and grant insight into specific elements that drive higher neophobic responses in this avian family group. VIDEO ABSTRACT.

Sex-specific effects of cooperative breeding and colonial nesting on prosociality in corvids.

The investigation of prosocial behavior is of particular interest from an evolutionary perspective. Comparisons of prosociality across non-human animal species have, however, so far largely focused on primates, and their interpretation is hampered by the diversity of paradigms and procedures used. Here, we present the first systematic comparison of prosocial behavior across multiple species in a taxonomic group outside the primate order, namely the bird family Corvidae. We measured prosociality in eight corvid species, which vary in the expression of cooperative breeding and colonial nesting. We show that cooperative breeding is positively associated with prosocial behavior across species. Also, colonial nesting is associated with a stronger propensity for prosocial behavior, but only in males. The combined results of our study strongly suggest that both cooperative breeding and colonial nesting, which may both rely on heightened social tolerance at the nest, are likely evolutionary pathways to prosocial behavior in corvids.

A novel test of flexible planning in relation to executive function and language in young children.

In adult humans, decisions involving the choice and use of tools for future events typically require episodic foresight. Previous studies suggest some non-human species are capable of future planning; however, these experiments often cannot fully exclude alternative learning explanations. Here, we used a novel tool-use paradigm aiming to address these critiques to test flexible planning in 3- to 5-year-old children, in relation to executive function and language abilities. In the flexible planning task, children were not verbally cued during testing, single trials avoided consistent exposure to stimulus-reward relationships, and training trials provided experience of a predictable return of reward. Furthermore, unlike most standard developmental studies, we incorporated short delays before and after tool choice. The critical test choice included two tools with equal prior reward experience-each only functional in one apparatus. We tested executive function and language abilities using several standardized tasks. Our results echoed standard developmental research: 4- and 5-year-olds outperformed 3-year-olds on the flexible planning task, and 5-year-old children outperformed younger children in most executive function and language tasks. Flexible planning performance did not correlate with executive function and language performance. This paradigm could be used to investigate flexible planning in a tool-use context in non-human species.

Decision-making flexibility in New Caledonian crows, young children and adult humans in a multi-dimensional tool-use task.

The ability to make profitable decisions in natural foraging contexts may be influenced by an additional requirement of tool-use, due to increased levels of relational complexity and additional work-effort imposed by tool-use, compared with simply choosing between an immediate and delayed food item. We examined the flexibility for making the most profitable decisions in a multi-dimensional tool-use task, involving different apparatuses, tools and rewards of varying quality, in 3-5-year-old children, adult humans and tool-making New Caledonian crows (Corvus moneduloides). We also compared our results to previous studies on habitually tool-making orangutans (Pongo abelii) and non-tool-making Goffin's cockatoos (Cacatua goffiniana). Adult humans, cockatoos and crows, but not children and orangutans, did not select a tool when it was not necessary, which was the more profitable choice in this situation. Adult humans, orangutans and cockatoos, but not crows and children, were able to refrain from selecting non-functional tools. By contrast, the birds, but not the primates tested, struggled to attend to multiple variables-where two apparatuses, two tools and two reward qualities were presented simultaneously-without extended experience. These findings indicate: (1) in a similar manner to humans and orangutans, New Caledonian crows and Goffin's cockatoos can flexibly make profitable decisions in some decision-making tool-use tasks, though the birds may struggle when tasks become more complex; (2) children and orangutans may have a bias to use tools in situations where adults and other tool-making species do not.

Delayed gratification in New Caledonian crows and young children: influence of reward type and visibility.

Self-control underlies cognitive abilities such as decision making and future planning. Delay of gratification is a measure of self-control and involves obtaining a more valuable outcome in the future by tolerating a delay or investing a greater effort in the present. Contextual issues, such as reward visibility and type, may influence delayed gratification performance, although there has been limited comparative investigation between humans and other animals, particularly non-primate species. Here, we adapted an automated 'rotating tray' paradigm used previously with capuchin monkeys to test for delay of gratification ability that requires little pre-test training, where the subject must forgo an immediate, less preferred reward for a delayed, more preferred one. We tested New Caledonian crows and 3-5-year-old human children. We manipulated reward types to differ in quality or quantity (Experiments 1 and 2) as well as visibility (Experiment 2). In Experiments 1 and 2, both species performed better when the rewards varied in quality as opposed to quantity, though performed above chance in both conditions. In Experiment 1, both crows and children were able to delay gratification when both rewards were visible. In Experiment 2, 5-year-old children outperformed 3- and 4-year olds, though overall children still performed well, while the crows struggled when reward visibility was manipulated, a result which may relate to difficulties in tracking the experimenters' hands during baiting. We discuss these findings in relation to the role of contextual issues on self-control when making species comparisons and investigating the mechanisms of self-control.

New Caledonian Crows Behave Optimistically after Using Tools.

Are complex, species-specific behaviors in animals reinforced by material reward alone or do they also induce positive emotions? Many adaptive human behaviors are intrinsically motivated: they not only improve our material outcomes, but improve our affect as well [1-8]. Work to date on animal optimism, as an indicator of positive affect, has generally focused on how animals react to change in their circumstances, such as when their environment is enriched [9-14] or they are manipulated by humans [15-23], rather than whether complex actions improve emotional state. Here, we show that wild New Caledonian crows are optimistic after tool use, a complex, species-specific behavior. We further demonstrate that this finding cannot be explained by the crows needing to put more effort into gaining food. Our findings therefore raise the possibility that intrinsic motivation (enjoyment) may be a fundamental proximate cause in the evolution of tool use and other complex behaviors. VIDEO ABSTRACT.

Negative emotional contagion and cognitive bias in common ravens (Corvus corax).

Emotional contagion is described as an emotional state matching between subjects, and has been suggested to facilitate communication and coordination in complex social groups. Empirical studies typically focus on the measurement of behavioral contagion and emotional arousal, yet, while highly important, such an approach often disregards an additional evaluation of the underlying emotional valence. Here, we studied emotional contagion in ravens by applying a judgment bias paradigm to assess emotional valence. We experimentally manipulated positive and negative affective states in demonstrator ravens, to which they responded with increased attention and interest in the positive condition, as well as increased redirected behavior and a left-eye lateralization in the negative condition. During this emotion manipulation, another raven observed the demonstrator's behavior, and we used a bias paradigm to assess the emotional valence of the observer to determine whether emotional contagion had occurred. Observers showed a pessimism bias toward the presented ambiguous stimuli after perceiving demonstrators in a negative state, indicating emotional state matching based on the demonstrators' behavioral cues and confirming our prediction of negative emotional contagion. We did not find any judgment bias in the positive condition. This result critically expands upon observational studies of contagious play in ravens, providing experimental evidence that emotional contagion is present not only in mammalian but also in avian species. Importantly, this finding also acts as a stepping stone toward understanding the evolution of empathy, as this essential social skill may have emerged across these taxa in response to similar socioecological challenges.

New Caledonian crows infer the weight of objects from observing their movements in a breeze.

Humans use a variety of cues to infer an object's weight, including how easily objects can be moved. For example, if we observe an object being blown down the street by the wind, we can infer that it is light. Here, we tested whether New Caledonian crows make this type of inference. After training that only one type of object (either light or heavy) was rewarded when dropped into a food dispenser, birds observed pairs of novel objects (one light and one heavy) suspended from strings in front of an electric fan. The fan was either on-creating a breeze which buffeted the light, but not the heavy, object-or off, leaving both objects stationary. In subsequent test trials, birds could drop one, or both, of the novel objects into the food dispenser. Despite having no opportunity to handle these objects prior to testing, birds touched the correct object (light or heavy) first in 73% of experimental trials, and were at chance in control trials. Our results suggest that birds used pre-existing knowledge about the behaviour exhibited by differently weighted objects in the wind to infer their weight, using this information to guide their choices.

New Caledonian Crows Use Mental Representations to Solve Metatool Problems.

One of the mysteries of animal problem-solving is the extent to which animals mentally represent problems in their minds. Humans can imagine both the solution to a problem and the stages along the way [1-3], such as when we plan one or two moves ahead in chess. The extent to which other animals can do the same is far less clear [4-25]. Here, we presented New Caledonian crows with a series of metatool problems where each stage was out of sight of the others and the crows had to avoid either a distractor apparatus containing a non-functional tool or a non-functional apparatus containing a functional tool. Crows were able to mentally represent the sub-goals and goals of metatool problems: crows kept in mind the location and identities of out-of-sight tools and apparatuses while planning and performing a sequence of tool behaviors. This provides the first conclusive evidence that birds can plan several moves ahead while using tools.

Function and flexibility of object exploration in kea and New Caledonian crows.

A range of non-human animals frequently manipulate and explore objects in their environment, which may enable them to learn about physical properties and potentially form more abstract concepts of properties such as weight and rigidity. Whether animals can apply the information learned during their exploration to solve novel problems, however, and whether they actually change their exploratory behaviour to seek functional information about objects have not been fully explored. We allowed kea (Nestor notabilis) and New Caledonian crows (Corvus moneduloides) to explore sets of novel objects both before and after encountering a task in which some of the objects could function as tools. Following this, subjects were given test trials in which they could choose among the objects they had explored to solve a tool-use task. Several individuals from both species performed above chance on these test trials, and only did so after exploring the objects, compared with a control experiment with no prior exploration phase. These results suggest that selection of functional tools may be guided by information acquired during exploration. Neither kea nor crows changed the duration or quality of their exploration after learning that the objects had a functional relevance, suggesting that birds do not adjust their behaviour to explicitly seek this information.

Behavioural Type Affects Space Use in a Wild Population of Crows (Corvus corone).

While personality-dependent dispersal is well studied, local space use has received surprisingly little attention in this context, despite the multiple consequences on survival and fitness. Regarding the coping style of individuals, recent studies on personality-dependent space use within a habitat indicate that 'proactive' individuals are wider ranging than 'reactive' ones. However, such studies are still scarce and cover limited taxonomic diversity, and thus, more research is needed to explore whether this pattern generalises across species. We examined the link between coping style and space use in a population of crows (Corvus corone) freely inhabiting the urban zoo of Vienna, Austria. We used a binary docility rating (struggle during handling vs. no struggle) and a tonic immobility test to quantify individual coping style. Individual space use was quantified as the number of different sites at which each crow was observed, and we controlled for different number of sightings per individual by creating a space use index. Only the binary docility rating showed repeatability over time, and significantly predicted space use. In contrast to previous studies, we found that reactive crows (no struggle during handling) showed wider ranging space use within the study site than proactive individuals (who struggled during handling). The discrepancy from previous results suggests that the relationship between behavioural type and space use may vary between species, potentially reflecting differences in socioecology.

Partner Choice in Raven (Corvus corax) Cooperation.

Although social animals frequently make decisions about when or with whom to cooperate, little is known about the underlying mechanisms of partner choice. Most previous studies compared different dyads' performances, though did not allow an actual choice among partners. We tested eleven ravens, Corvus corax, in triads, giving them first the choice to cooperate with either a highly familiar or a rather unfamiliar partner and, second, with either a friend or a non-friend using a cooperative string-pulling task. In either test, the ravens had a second choice and could cooperate with the other partner, given that this one had not pulled the string in the meantime. We show that during the experiments, these partner ravens indeed learn to wait and inhibit pulling, respectively. Moreover, the results of these two experiments show that ravens' preferences for a specific cooperation partner are not based on familiarity. In contrast, the ravens did show a preference based on relationship quality, as they did choose to cooperate significantly more with friends than with non-friends and they were also more proficient when cooperating with a friend. In order to further identify the proximate mechanism of this preference, we designed an open-choice experiment for the whole group where all birds were free to cooperate on two separate apparatuses. This set-up allowed us to distinguish between preferences for close proximity and preferences to cooperate. The results revealed that friends preferred staying close to each other, but did not necessarily cooperate with one another, suggesting that tolerance of proximity and not relationship quality as a whole may be the driving force behind partner choice in raven cooperation. Consequently, we stress the importance of experiments that allow such titrations and, suggest that these results have important implications for the interpretations of cooperation studies that did not include open partner choice.

Socially Driven Consistent Behavioural Differences during Development in Common Ravens and Carrion Crows.

Consistent individual differences in behaviour, or 'personality', are likely to be influenced by development, social context, and species ecology, though few comparative, longitudinal studies exist. Here, we investigated the role of development and social context on personality variation in two identically reared, social corvids: common ravens and carrion crows. We repeatedly presented subjects with a variety of novel food and objects, while alone and in a primarily sibling subgroup, from fledging to sub-adulthood. We predicted that consistent individual differences would emerge later in development, and that conspecific presence would facilitate behavioural similarities. In contrast to our predictions, we found that individuals of both species were highly inconsistent in their behavioural responses throughout the development period. In line with our predictions, though in the ravens only, conspecific presence promoted behavioural similarities as individuals were strongly shaped by their subgroup, and it is likely that these effects were driven by social context rather than relatedness. We discuss these findings in relation to developmental steps and the role of social relations in these species. Overall, our findings highlight that these two species are highly adaptable in their behaviour, and the ravens in particular are strongly influenced by their social environment, which may facilitate cooperation and social learning.

Prosthesis Control with an Implantable Multichannel Wireless Electromyography System for High-Level Amputees: A Large-Animal Study.

BACKGROUND: Myoelectric prostheses lack a strong human-machine interface, leading to high abandonment rates in upper limb amputees. Implantable wireless electromyography systems improve control by recording signals directly from muscle, compared with surface electromyography. These devices do not exist for high amputation levels. In this article, the authors present an implantable wireless electromyography system for these scenarios tested in Merino sheep for 4 months. METHODS: In a pilot trial, the electrodes were implanted in the hind limbs of 24 Sprague-Dawley rats. After 8 or 12 weeks, impedance and histocompatibility were assessed. In the main trial, the system was tested in four Merino sheep for 4 months. Impedance of the electrodes was analyzed in two animals. Electromyographic data were analyzed in two freely moving animals repeatedly during forward and backward gait. RESULTS: Device implantation was successful in all 28 animals. Histologic evaluation showed a tight encapsulation after 8 weeks of 78.2 ± 26.5 µm subcutaneously and 92.9 ± 31.3 µm on the muscular side. Electromyographic recordings show a distinct activation pattern of the triceps, brachialis, and latissimus dorsi muscles, with a low signal-to-noise ratio, representing specific patterns of agonist and antagonist activation. Average electrode impedance decreased over the whole frequency range, indicating an improved electrode-tissue interface during the implantation. All measurements taken over the 4 months of observation used identical settings and showed similar recordings despite changing environmental factors. CONCLUSION: This study shows the implantation of this electromyography device as a promising alternative to surface electromyography, providing a potentially powerful wireless interface for high-level amputees.

Subadult ravens generally don't transfer valuable tokens to conspecifics when there is nothing to gain for themselves.

The extent to which humans help each other is extraordinary in itself, and difficult to explain from an evolutionary perspective. Therefore, there has been a recent surge in studies investigating the evolution of prosocial behavior using a comparative approach. Nevertheless, most of these studies have focused on primates only, and little is known about other animal orders. In a previous study, common ravens (Corvus corax) have been shown to be indifferent to the gains of conspecifics. However, this may have been due to the experimental set-up, as many studies that use different set-ups report conflicting results within the same species. We therefore tested ravens' prosocial tendencies in a different set-up; i.e., we tested whether sub-adult ravens would transfer a token to a partner and, thereby, provide the partner with the opportunity to exchange a token for a reward. To control and test for effects of partner identity, we tested eight individuals both in a dyadic and in a group setting. Our results show that in general the ravens in our experiment did not show other-regarding preferences. However, some acts of helping did occur spontaneously. We discuss what could be the causes for those sporadic instances, and why in general prosocial tendencies were found to be almost lacking among the ravens in this set-up.

Tolerance and Social Facilitation in the Foraging Behaviour of Free-Ranging Crows (Corvus corone corone; C. c. cornix).

Social foraging provides animals with opportunities to gain knowledge about available food. Studies indicate that animals are influenced by social context during exploration and are able to learn socially. Carrion and hooded crows, which are opportunistic generalists with flexible social systems, have so far received little focus in this area. We combined observational and experimental approaches to investigate social interactions during foraging and social influences on crow behaviour within a free-ranging population at Vienna Zoo, which included 115 individually marked crows. We expected the crows to be tolerant of conspecifics during foraging due to high food abundance. We predicted that social context would enhance familiar object exploration, as well as a specific foraging strategy: predation by crows on other species. We found that crows were highly tolerant of one another, as reflected by their high rates of cofeeding - where they fed directly beside conspecific(s) - relative to affiliative or agonistic interactions. Evidence for social facilitation - when the observer's behaviour is affected by the mere presence of a model - was found in both object exploration and predation behaviour. Specifically, crows touched the objects more frequently when others were present (whilst only approaching the objects when alone), and conspecifics were present more frequently during predation events involving the high-risk target species. Evidence for enhancement during object exploration - where the observer's attention is drawn to a place or object by a model's actions - was not confirmed in this context. Our results highlight the role played by the presence of conspecifics across different contexts: natural foraging behaviour, familiar object exploration and a specific foraging strategy. To our knowledge, this is one of the first corvid studies aimed at teasing apart specific social influence and learning mechanisms in the field. These crows therefore make promising candidates for studying social learning and its consequences under naturalistic conditions.