Cleaner fish cause predators to reduce aggression toward bystanders at cleaning stations
2008, Cheney, Karen L., Bshary, Redouan, Grutter, Alexandra S.
Mutualisms, in which both participants gain a net benefit, are ubiquitous in all ecosystems, and the importance of understanding their broader ecological context has been demonstrated many times. Indirect effects of mutualisms may have important implications for surrounding ecosystems through changes in density, species composition, or behavior; however, the latter has been difficult to quantify. In fish cleaning mutualisms, cleaners benefit by removing and consuming ectoparasites from clients, whereas clients benefit from a reduction in parasite load. Cleaner fish are also thought to benefit from immunity to predation and use tactile stimulation as a preconflict management strategy to manipulate partners' decisions and to avoid being eaten by piscivorous client fish. Here we show, using a laboratory experiment, that the presence of cleaner fish resulted in nearby fish not involved in the cleaner–client mutualism experiencing less aggression (chases) from predatory clients. In addition, the rate that piscivorous clients chased prey was negatively correlated with the amount of tactile stimulation given to the predator by the cleaner. These data suggest that, in the laboratory, the risk of aggression from predators toward nearby prey fish was greatly reduced as a by-product of cleaner fish presence and tactile stimulation of predators by cleaner fish. These results raise the question of whether cleaning stations act as safe havens from predator aggression.
Cleaner wrasse prefer client mucus : support for partner control mechanisms in cleaning interactions
2003-11-07, Grutter, Alexandra S., Bshary, Redouan
Recent studies on cleaning behaviour suggest that there are conflicts between cleaners and their clients over what cleaners eat. The diet of cleaners usually contains ectoparasites and some client tissue. It is unclear, however, whether cleaners prefer client tissue over ectoparasites or whether they include client tissue in their diet only when searching for parasites alone is not profitable. To distinguish between these two hypotheses, we trained cleaner fish Labroides dimidiatus to feed from plates and offered them client mucus from the parrotfish Chlorurus sordidus, parasitic monogenean flatworms, parasitic gnathiid isopods and boiled flour glue as a control. We found that cleaners ate more mucus and monogeneans than gnathiids, with gnathiids eaten slightly more often than the control substance. Because gnathiids are the most abundant ectoparasites, our results suggest a potential for conflict between cleaners and clients over what the cleaner should eat, and support studies emphasizing the importance of partner control in keeping cleaning interactions mutualistic.
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.
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.