Adjustments of levels of cooperation in cleaner wrasse "Labroides dimidiatus": the effects of an audience and satiation
2015, Pinto, Ana Isabel, Bshary, Redouan
La coopération, soit l’entraide entre individus sans lien de parenté, est une énigme évolutive. Cela est dû au fait que l’aide est souvent un investissement qui doit générer des avantages futurs pour pouvoir faire l’objet d’une sélection positive. Généralement, la sélection naturelle favorise les individus qui adoptent un comportement égoïste. La tricherie devient donc une question conceptuelle majeure. Cependant, les exemples de coopération sont nombreux dans la nature. De ce fait, la recherche d'explications réconciliant la coopération avec la théorie de l'évolution a longtemps été d’une importance majeure en biologie, mais également dans les sciences sociales, l’objectif étant d'expliquer la complexité sociale chez l'homme. Divers mécanismes dits de contrôle du partenaire - des réponses comportementales qui entraînent une réduction des gains d'un partenaire tricheur de sorte qu'un partenaire coopérant gagne davantage - se sont avérés efficaces pour stabiliser la coopération. Mes recherches sur ce sujet ce sont axées en particulier sur le rôle du prestige social dans un réseau de communication. En effet, de nombreuses interactions animales sont observées par des tiers («spectateurs»), qui peuvent obtenir des informations extrêmement utiles sur les interactants. Dans le contexte de la coopération, les spectateurs doivent ainsi essayer d'identifier des individus singulièrement coopératifs comme futurs partenaires, ce qui permet de sélectionner les individus particulièrement coopératifs s'ils sont observés.
Mon système modèle a consisté d’un mutualisme de nettoyage marin impliquant des labres nettoyeurs (Labroides dimidiatus) et ses poissons de récif dit «clients» qui leur rendent visite pour se faire enlever les ectoparasites. Cependant, des conflits surgissent car les nettoyeurs préfèrent la couche de mucus protectrice des clients aux ectoparasites, où se nourrir de mucus est préjudiciable au client et est donc fonctionnellement considéré comme de la tricherie. Par conséquent, les clients doivent faire en sorte que les nettoyeurs mangent contre leur préférence afin de pouvoir bénéficier d'un bon service de nettoyage. Des observations sur le terrain et une expérience de laboratoire utilisant des plaques en plexiglas en remplacement de clients avaient déjà suggéré que les clients spectateurs étaient attentifs à la manière dont un nettoyeur traite son client actuel et que les nettoyeurs sont plus coopératifs s’ils sont observés. J'ai pu démontrer ce concept de prestige social pour la première fois dans le cadre d'une expérience de laboratoire contrôlée utilisant de véritables interactions client-nettoyeur. Dans deux autres expériences utilisant soit des plaques en plexiglas soit de vrais clients, j'ai montré que les nettoyeurs peuvent ajuster la qualité de leurs services à l'importance relative du client actuel par rapport au client spectateur: plus le spectateur a de la valeur, plus le service envers le client actuel est peaufiné. Dans une troisième expérience, j’ai manipulé le niveau de satiété des nettoyeurs afin de tester la prédiction de la théorie du marché biologique selon laquelle un besoin d’interactions temporairement faible entraîne une baisse de la qualité du service. De manière quelque peu surprenante, cette prédiction n’a pas été confirmée, les nettoyeurs rassassiés ayant augmenté leur niveau de coopération envers leurs clients, c’est-à-dire qu’ils ont moins triché lors des interactions avec leurs clients et se sont nourris davantage contre leur préférence sur les plaques en plexiglas. Ainsi, les nettoyeurs rassassiés investissent fonctionnellement dans leur relation avec les clients pour des avantages futurs.
En conclusion, mon travail de recherche démontre que le labre nettoyeur L. dimidiatus, est capable de prendre des décisions sophistiquées, adaptées aux spécificités de la situation. Les résultats soulèvent des questions concernant les processus cognitifs sous-jacents, car ils remettent en cause la notion selon laquelle des cerveaux plus larges sont nécessaires pour une coopération sophistiquée. Au lieu de cela, il semble qu'une approche écologique par rapport à la cognition soit plus appropriée pour expliquer mes résultats. Mon étude s'inscrit dans une longue tradition selon laquelle les poissons constituent des systèmes modèles idéaux pour tester la théorie de la coopération, dont les résultats prometteurs devraient inspirer de nouvelles analyses théoriques., Cooperation, the mutual helping between unrelated individuals, is an evolutionary puzzle. This is because helping is often an investment that must yield future benefits in order to be under positive selection. Generally, natural selection favours individuals that perform self-serving behaviour, and hence cheating is a major conceptual issue. However, examples of cooperation are abundant in nature. As such, finding explanations that reconcile cooperation with evolutionary theory has long been a major focus in biology but also in the social sciences with their aim to explain the social complexity in humans. A variety of so-called partner control mechanisms – behavioural responses that cause a reduction in the payoffs of a cheating partner such that a cooperating partner gains more – have been shown to stabilise cooperation. My research has focused in particular on the role of social prestige in a communication network. Many animal interactions are observed by third parties (“bystanders”), who may gain valuable information about the interactants. In the context of cooperation, bystanders should try to identify particularly cooperative individuals as future partners, which selects for individuals being particularly cooperative if they are observed.
My model system has been marine cleaning mutualism involving bluestreak cleaner wrasses (Labroides dimidiatus) and their so-called “client” reef fishes that visit to have ectoparasites removed. However, conflict arises as cleaners prefer the protective mucus layer of clients over ectoparasites, where mucus feeding is detrimental to the client and hence functionally constitutes cheating. Thus, clients have to make cleaners feed against their preference in order to receive a good cleaning service. Field observations and a laboratory experiment using Plexiglas plates as client surrogates had already suggested that bystander clients pay attention to how a cleaner treats its current client, and that cleaners are more cooperative if observed. I could demonstrate this social prestige concept for the first time in a controlled laboratory experiment in real cleaner-client interactions. In two further experiments using either plates or real clients I showed that cleaners can fine-tune their service quality to the relative importance of current client versus bystander: the more valuable the bystander the better the current service. Finally, I manipulated the cleaners’ level of satiation in order to test the prediction from biological market theory that a temporarily low need for interactions causes a decrease in service quality. Somewhat surprisingly, this prediction was not met as satiated cleaners increased their cooperation levels towards their clients, i.e. they caused less jolts during interactions with their clients and fed more against their preference on plates. Thus, satiated cleaners functionally invest into their relationship with clients for future benefits.
In conclusion, my work shows that cleaner wrasse L. dimidiatus show sophisticated decision rules that are fine-tuned to the specifics of the situation. The results raise questions concerning the underlying cognitive processes as they challenge the notion that large brains are necessary for sophisticated cooperation. Instead, it appears that an ecological approach to cognition is better suited to explain my results. My study fits into a long tradition that fish yield ideal model systems to test cooperation theory, where results hopefully inspire further theoretical analyses.
Punishment and partner switching cause cooperative behaviour in a cleaning mutualism
2005, Bshary, Redouan, Grutter, Alexandra S.
What are the mechanisms that prevent partners from cheating in potentially cooperative interactions between unrelated individuals? The cleaner fish Labroides dimidiatus and client reef fish both benefit from an interaction as long as the cleaner eats ectoparasites. However, the cleaner fish prefers some client mucus, which constitutes cheating. Field observations suggested that clients control such cheating by using punishment (chasing the cleaner) or by switching partners (fleeing from the cleaner). Here, we tested experimentally whether such client behaviours result in cooperative cleaner fish. Cleaners were allowed to feed from Plexiglas plates containing prawn items and fish flake items. A lever attached to the plates allowed us to mimic the behaviours of clients. As cleaners showed a strong preference for prawn over flakes, we taught them that eating their preferred food would cause the plate to either chase them or to flee, while feeding on flakes had no negative consequences. We found a significant shift in cleaner fish foraging behaviour towards flake feeding after six learning trials. As punishment and terminating an interaction resulted in the cleaners feeding against their preferences in our experiment, we propose that the same behaviours in clients improve the service quality of cleaners under natural conditions.
Indo-Pacific parrotfish exert partner choice in interactions with cleanerfish but Caribbean parrotfish do not
, Soares, Marta C, Cardoso, Sónia C, Nicolet, Katia J, Côté, Isabelle M, Bshary, Redouan
Cooperation theory puts a strong emphasis on partner control mechanisms that have evolved to stabilize cooperation against the temptation of cheating. The marine cleaning mutualism between the Indo-Pacific bluestreack cleaner wrasse, Labroides dimidiatus, and its reef fish ‘clients’ has been a model system to study partner control mechanisms and counterstrategies. These cleaners cooperate by eating ectoparasites; however, they can cheat by taking client mucus, which they prefer. Such a conflict may be the exception. For example, Caribbean cleaning gobies, Elacatinus spp., prefer to eat ectoparasites instead of mucus. While partner control mechanisms and counterstrategies seem to be absent in cleaning gobies, no study has directly compared cleaner wrasses and cleaning gobies by using the same methods. We examined systematic differences in cleaning interaction patterns and strategic behaviour exhibited by 12 closely related parrotfish species in the two systems. Parrotfish seeking cleaner wrasses visited them more often and spent more time with their cleaner than parrotfish seeking cleaning gobies. Moreover, the clients of cleaner wrasses returned more often to the same cleaner following a positive interaction, whereas the clients of cleaning gobies were less influenced by the outcome of previous interactions. We hypothesize that the higher frequency and repeated nature of interactions observed in the cleaner wrasse system, combined with the need to resolve conflicts, might have been prerequisites for the development of complex behavioural strategies.
Strategic adjustment of service quality to client identity in the cleaner shrimp, Periclimenes longicarpus
2009, Chapuis, Lucille, Bshary, Redouan
Cleaning mutualism, in which cleaning organisms remove ectoparasites from cooperating ‘clients’, is widespread among marine animals. Until now, research has focused on fishes as cleaners, whereas cleaner shrimps have received little attention. The aim of this study was to investigate the cleaning behaviour of the cleaner shrimp, Periclimenes longicarpus, and to compare the results directly to data on the sympatric and well-studied cleaner wrasse, Labroides dimidiatus. We first compared the time spent cleaning and client diversity as indicators of the potential importance of the cleaner shrimp to client health and found strong similarities between shrimp and wrasse. We further looked at three correlates of service quality: duration of interactions, tactile stimulation of clients, and jolt rates as correlates of mucus feeding (=cheating). We specifically predicted that shrimps would cheat clients less frequently than the wrasses because they should be more vulnerable to aggressive responses by clients. Although the results partly support our hypothesis, they also suggest that both species strategically adjust cheating rates according to risk, as predatory clients jolted less frequently than nonpredatory clients. In conclusion, the results suggest that the shrimps play an important role in client health but that nonpredatory clients have to control the shrimps' behaviour to receive a good service.
From parasitism to mutualism: partner control in asymmetric interactions
2002, Johnstone, Rufus, Bshary, Redouan
Intraspecific cooperation and interspecific mutualism often feature a marked asymmetry in the scope for exploitation. Cooperation may nevertheless persist despite one-sided opportunities for cheating, provided that the partner vulnerable to exploitation has sufficient control over the duration of interaction. Here we develop a simple, game theoretical model of this form of partner control. We show that as a victim's ability to terminate an encounter increases, selection can favour reduced exploitation, resulting in a switch from parasitism to mutualism. For a given level of control, exploitation is likely to be less intense and the interaction to last longer when there are greater mutualistic benefits to be gained, and when the benefits of cheating are lower relative to the costs inflicted on the victim. Observations of interactions between cleaner-fish and non-predatory species of client are shown to match these predictions.
Mutualism, market effects and partner control
2008, Johnstone, Rufus A., Bshary, Redouan
Intraspecific cooperation and interspecific mutualism often feature a marked asymmetry in the scope for exploitation. Cooperation may nevertheless persist despite one-sided opportunities for cheating, provided that the partner vulnerable to exploitation has sufficient control over the duration of interaction. The effectiveness of the threat of terminating an encounter, however, depends upon the ease with which both the potential victim and the potential exploiter can find replacement partners. Here, we extend a simple, game-theoretical model of this form of partner control to incorporate variation in the relative abundance of potential victims and exploiters, which leads to variation in the time required for individuals of each type to find a new partner. We show that such market effects have a dramatic influence on the stable level of exploitation (and consequent duration of interaction). As the relative abundance of victims decreases, they become less tolerant to exploitation, terminating encounters earlier (for a given level of exploitation), whereas exploiters behave in a more cooperative manner. As a result, the stable duration of interaction actually increases, despite the decreasing tolerance of the victims. Below a critical level of relative victim abundance, the model suggests that the cost of finding a replacement partner becomes so great that it does not pay to exploit at all.
Cleaner fish Labroides dimidiatus manipulate client reef fish by providing tactile stimulation
2001, Bshary, Redouan, Wurth, Manuela
The cleaner wrasse Labroides dimidiatus often touches 'client' reef fish dorsal fin areas with its pelvic and pectoral fins. The relative spatial positions of cleaner and client remain constant and the cleaner's head points away from the client's body. Therefore, this behaviour is not compatible with foraging and the removal of client ectoparasites. As clients seek such 'tactile stimulation', it can be classified as an interspecific socio-positive behaviour. Our field observations on 12 cleaners (observation time of 112 h) suggest that cleaners use tactile stimulation in order to successfully (i) alter client decisions over how long to stay for an inspection, and (ii) stop clients from fleeing or aggressive chasing of the cleaner in response to a cleaner fish bite that made them jolt. Finally predatory clients receive tactile stimulation more often than non-predatory clients, which might be interpreted as an extra service that cleaners give to specific partners as pre-conflict management, as these partners would be particularly dangerous if they started a conflict. We therefore propose that cleaner fish use interspecific social strategies, which have so far been reported only from mammals, particularly primates.