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Dominance is associated with reduced cleaning activity in group-living Elacatinus prochilos gobies

2023, Mazzei Cespe Barbosa, Renata, Emery, Yasmin, Marta C. Soares, Bshary, Redouan

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Juvenile cleaner fish can socially learn the consequences of cheating

2020, Noa Truskanov, Emery, Yasmin, Bshary, Redouan

Social learning is often proposed as an important driver of the evolution of human cooperation. In this view, cooperation in other species might be restricted because it mostly relies on individually learned or innate behaviours. Here, we show that juvenile cleaner fish (Labroides dimidiatus) can learn socially about cheating consequences in an experimental paradigm that mimics cleaners’ cooperative interactions with client fish. Juvenile cleaners that had observed adults interacting with model clients learned to (1) behave more cooperatively after observing clients fleeing in response to cheating; (2) prefer clients that were tolerant to cheating; but (3) did not copy adults’ arbitrary feeding preferences. These results confirm that social learning can play an active role in the development of cooperative strategies in a non-human animal. They further show that negative responses to cheating can potentially shape the reputation of cheated individuals, influencing cooperation dynamics in interaction networks.

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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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Configural learning by cleaner fish in a complex biological market task

2021, Noa Truskanov, Emery, Yasmin, Miquel Porta, Bshary, Redouan

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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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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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Brain morphology predicts social intelligence in wild cleaner fish

2020, Triki, Zegni, Magda C. Teles, Emery, Yasmin, Rui F. Oliveira, Bshary, Redouan

It is generally agreed that variation in social and/or environmental complexity yields variation in selective pressures on brain anatomy, where more complex brains should yield increased intelligence. While these insights are based on many evolutionary studies, it remains unclear how ecology impacts brain plasticity and subsequently cognitive performance within a species. Here, we show that in wild cleaner fish (Labroides dimidiatus), forebrain size of high-performing individuals tested in an ephemeral reward task covaried positively with cleaner density, while cerebellum size covaried negatively with cleaner density. This unexpected relationship may be explained if we consider that performance in this task reflects the decision rules that individuals use in nature rather than learning abilities: cleaners with relatively larger forebrains used decision-rules that appeared to be locally optimal. Thus, social competence seems to be a suitable proxy of intelligence to understand individual differences under natural conditions.

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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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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.