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Long‐term memory retention in a wild fish species “Labroides dimidiatus” eleven months after an aversive event

2019-10, Triki, Zegni, Bshary, Redouan

Memory is essential to enhance future survival and reproduction as it helps in storing and retrieving useful information to solve particular environmental problems. However, we lack quantitative evidence on how far animals in the wild can maintain given information for extended periods without reinforcement. Here, we document correlative evidence of cleaner fish Labroides dimidiatus remembering being caught in a barrier net for up to 11 months. In 2015, about 60% of cleaners from one large isolated reef had been used for laboratory experiments and then returned to their site of capture. Eleven months later, 50% of cleaners at the same site showed an unusual hiding response to the placement of the barrier net, in contrast to three control sites where no cleaners had been caught during the last 2 years. The results suggest that a single highly aversive event (i.e., being caught in a barrier net) resulted in cleaners storing long‐term crucial information that allowed them to avoid being caught again. Our results further our knowledge of fish cognitive capacities and long‐term memory retention.

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Social-learning abilities of wild vervet monkeys in a two-step task artificial fruit experiment

2011, van de Waal, Erica, Bshary, Redouan

Social learning is the basis for the formation of traditions in both human and nonhuman animals. Field observations and experiments provide evidence for the existence of traditions in animals but they do not address the underlying social-learning mechanisms. We used an established laboratory experimental paradigm, the artificial fruit design, to test for copying of a sequence of actions and local enhancement in six groups of wild vervet monkeys, Chlorocebus aethiops. We introduced a two-step task where models had to remove a bar to untie a rope that blocked a single door of a box. The models were high-ranking individuals that monopolized the box early on and discovered by trial and error how to open it. We obtained successful models in three groups, while the other three groups acted as controls. After 20 successful demonstrations, we tested subjects with a box that had a rope in the same position but the rope was not functional. Under these conditions, sequential copying of the two-step opening did not occur. Only individuals that were exposed to models were likely to touch the bar if door opening was not immediately successful, providing evidence for local enhancement. When we presented the boxes with the functional rope, we found no effect of having been exposed to a model on the probability that subjects solved the task. We conclude that the social-learning abilities of wild vervet monkeys are relatively limited and discuss potential problems concerning the technical difficulty of the task.

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The effect of innovation and sex-specific migration on neutral cultural differentiation

2011, Yeaman, Samuel, Bshary, Redouan, Lehmann, Laurent

Studies of behaviour are increasingly focusing on acquisition of traits through cultural inheritance. Comparison of patterns of spatial population structure (FST) between neutral genetic loci and behavioural or cultural traits can been used to test hypotheses about demography, life history, and the mechanisms of inheritance/transmission of these traits in humans, chimpanzees and other animals. Here, we develop analytical expectations to show how FST in cultural traits can differ strongly from that measured at neutral genetic markers if migration is largely restricted to one sex but social learning is predominantly modelled on the other (e.g. males migrate, females serve as models for cultural traits), if one individual is the learning model for many, or if rates of innovation (individual learning) are high or rates of social learning are low. We discuss how comparisons of FST between genetic loci and behavioural traits can be applied to evaluate the importance of innovation in shaping patterns of cultural differentiation, as even low rates of innovation can considerably reduce FST, relative to observed structure at neutral genetic loci. Our results also suggest that differentiation in neutral cultural traits should occur over much smaller scales in species with male migration and female enculturation (or the reverse).

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Interactions Between Sabre-Tooth Blennies and Their Reef Fish Victims: Effects Of Enforced Repeated Game Structure and Local Abundance on Victim Aggression

2010, Bshary, Andrea, Bshary, Redouan

The conditions under which humans benefit from contributing to a public good have attracted great interest; in particular the potential role of punishment of cheaters is hotly debated. In contrast, similar studies on other animals are lacking. In this study, we describe for the first time how the course of interactions between parasitic sabre-tooth blennies (the cheaters) and their reef fish victims can be used to study both punishment and the emergence of public goods. Sabre tooth blennies (Plagiotremus sp.) sneak up from behind to bite off small pieces of scales and/or mucus from other fish. Victims regularly show spontaneous aggression as well as aggressive responses to blenny attacks. In a between species comparison, we tested how the probability of chasing a blenny is affected by (1) the option of avoiding interactions with a blenny by avoiding its small territory, and (2) variation in local abundance of conspecifics. We found that resident victim species are more aggressive towards blennies than visiting species. This difference persisted when we controlled for victim size and territoriality, suggesting that it is the enforced repeated game structure that causes residents to chase blennies. In residents, we also found a negative correlation between aggression towards blennies and local abundance, which suggests that the benefits of chasing are diluted with increasing local abundance. We discuss the implication of these results for future studies.

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Endogenous oxytocin predicts helping and conversation as a function of group membership.

2018-07-04T00:00:00Z, McClung, Jennifer Susan, Triki, Zegni, Clément, Fabrice, Bangerter, Adrian, Bshary, Redouan

Humans cooperate with unrelated individuals to an extent that far outstrips any other species. We also display extreme variation in decisions about whether to cooperate or not, and the mechanisms driving this variation remain an open question across the behavioural sciences. One candidate mechanism underlying this variation in cooperation is the evolutionary ancient neurohormone oxytocin (OT). As current research focuses on artificial administration of OT in asocial tasks, little is known about how the hormone in its naturally occurring state actually impacts behaviour in social interactions. Using a new optimal foraging paradigm, the 'egg hunt', we assessed the association of endogenous OT with helping behaviour and conversation. We manipulated players' group membership relative to each other prior to an egg hunt, during which they had repeated opportunities to spontaneously help each other. Results show that endogenous baseline OT predicted helping and conversation type, but crucially as a function of group membership. Higher baseline OT predicted increased helping but only between in-group players, as well as decreased discussion about individuals' goals between in-group players but conversely more of such discussion between out-group players. Subsequently, behaviour but not conversation during the hunt predicted change in OT, in that out-group members who did not help showed a decrease in OT from baseline levels. In sum, endogenous OT predicts helping behaviour and conversation, importantly as a function of group membership, and this effect occurs in parallel to uniquely human cognitive processes.

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Variable responses of hawkmoths to nectar-depleted plants in two native Petunia axillaris (Solanaceae) populations

2011, Brandenburg, Anna, Bshary, Redouan

Pollination success of deceptive orchids is affected by the density and distribution of nectar providing plant species and overall plant density. Here we extended the framework of how plant density can affect pollination to examine how it may promote the success of plant intraspecific cheaters. We compared hawkmoth behaviour in two native populations of Petunia axillaris, where we simultaneously offered rewarding and manually depleted P. axillaris. We asked whether pollinator foraging strategies change as a function of plant density and whether such changes may differentially affect nectarless plants. We observed the first choice and number of flowers visited by pollinators and found that in the dense population, pollinators visited more flowers on rewarding plants than on nectar-depleted plants. In the sparse population, such discrimination was absent. As we found no differences in nectar volume between plants of the two populations, the observed differences in plant density may be temporal. We reason that if differences were more permanent, an equivalent of the remote habitat hypothesis prevails: in a sparse population, cheating plants benefit from the absence of inter- and intraspecific competitors because pollinators tend to visit all potential resources. In a denser population, a pollinator’s optimal foraging strategy involves more selectivity. This would cause between-plant competition for pollinators in a pollinator-limited context, which applies to most hawkmoth-pollinated systems. We propose that nectar-provisioning of plants can be density-dependant, with cheaters able to persist in low density areas.

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A General Scheme to Predict Partner Control Mechanisms in Pairwise Cooperative Interactions Between Unrelated Individuals

2011, Bshary, Redouan, Bronstein, Judith L.

Recent years have seen an explosion in the diversity of partner control mechanisms hypothesised to stabilise cooperative behaviour among unrelated individuals. Game theory suggests numerous strategies, each with specific decision rules that allow cooperators to control a non-contributing partner. This diversity of hypothetical strategies seems likely to reflect diversity in the types of intraspecific cooperation and interspecific mutualism that exist in nature. It is therefore important to provide a framework that explains similarities and differences between the various hypothetical strategies and that predicts how key parameters that describe the natural history of natural systems favour different control mechanisms. We develop a novel unifying framework for pairwise interactions between unrelated individuals, in which we link specific control mechanisms to specific game structures. The latter are defined by unique combinations of the states of five parameters that describe investment, aspects of the payoff matrix, the number of interactions and partner choice. We find that specific control mechanisms potentially have utility in a limited number of game structures; conversely, each game structure may typically offer a few competing control mechanisms. Our framework offers theoreticians specific problems that await mathematical exploration, while at the same time offering empiricists guidelines for evaluating the game structure and corresponding control mechanisms in their systems.

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The language of cooperation: shared intentionality drives variation in helping as a function of group membership

2017-8-27, McClung, Jennifer Susan, Placi, Sarah, Bangerter, Adrian, Clément, Fabrice, Bshary, Redouan

While we know that the degree to which humans are able to cooperate is unrivalled by other species, the variation humans actually display in their cooperative behaviour has yet to be fully explained. This may be because research based on experimental game-theoretical studies neglects fundamental aspects of human sociality and psychology, namely social interaction and language. Using a newoptimal foraging game loosely modelled on the prisoner’s dilemma, the Egg Hunt, we categorized players as either in-group or out-group to each other and studied their spontaneous language usage while they made interactive, potentially cooperative decisions. Both shared group membership and the possibility to talk led to increased cooperation and overall success in the hunt. Notably, analysis of players’ conversations showed that in-group members engaged more in shared intentionality, the human ability to both mentally represent and then adopt another’s goal, whereas out-group members discussed individual goals more. Females also helped more and displayed more shared intentionality in discussions than males. Crucially, we show that shared intentionality was the mechanism driving the increase in helping between in-group players over out-group players at a cost to themselves. By studying spontaneous language during social interactions and isolating shared intentionality as the mechanism underlying successful cooperation, the current results point to a probable psychological source of the variation in cooperation humans display.

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Short-Term Variation in the Level of Cooperation in the Cleaner Wrasse Labroides dimidiatus: Implications for the Role of Potential Stressors

2011, Bshary, Redouan, Oliveira, Rui F., Grutter, Alexandra S.

There is a wealth of game theoretical approaches to the evolution and maintenance of cooperation between unrelated individuals and accumulating empirical tests of these models. This contrasts strongly with our lack of knowledge on proximate causes of cooperative behaviour. Marine cleaning mutualism has been used as a model system to address functional aspects of conflict resolution: client reef fish benefit from cleaning interactions through parasite removal, but cleaner fish Labroides dimidiatus prefer client mucus. Hence, feeding against their preference represents cooperative behaviour in cleaners. Cleaners regularly cheat non-predatory clients while they rarely cheat predatory clients. Here, we asked how precisely cleaners can adjust service quality from one interaction to the next. We found that non-predatory clients receive a better service if the previous client was a predator than if the previous client was a non-predator. In a related laboratory experiment, a hand-net used as a stressor resulted in cleaners feeding more against their preference in subsequent interactions. The combination of the cleaners’ behaviour in the two studies shows that the cleaners’ service quality for a given client species is not fixed, but it can be manipulated. The results suggest that short-term stress is one factor that causes cleaners to increase their levels of cooperation, a hypothesis that is amenable to further experiments manipulating the endocrine system.

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Cooperation and deception: from evolution to mechanisms

2010, Brosnan, Sarah F., Bshary, Redouan

Nature is full of struggle, as predicted by the theory of evolution through natural selection, yet there are also paramount examples where individuals help each other. These instances of helping have been difficult to reconcile with Darwin's theory because it is not always obvious how individuals are working for their own direct benefit. Consequently, initial publications that offered solutions to subsets of the observed cases of helping, such as kin selection or reciprocity, are among the most influential and most cited papers in evolution/behavioural ecology. During the last few years, a wave of new studies and concepts has considerably advanced our understanding of the conditions under which individuals are selected to help others. On the empirical side, advances are due to stronger incorporation of the natural history of each study species and an emphasis on proximate questions regarding decision-making processes. In parallel, theorists have provided more realistic models together with an increased exploration of the importance of life history and ecology in understanding cooperation. The ideas presented by the authors of this volume represent, in many ways, the revolutionary new approach to studying behaviour which is currently underway.