Punishment and partner switching cause cooperative behaviour in a cleaning mutualism

Abstract

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.

Altruism in insect societies and beyond: voluntary or enforced?

“…For example, the cleaner fish Labroides dimidiatus eats ectoparasites on its client reef fish but could also cheat by eating client tissue or mucus. Clients use three different mechanisms to enforce cooperation: (i) they avoid cleaners that have been observed cheating (partner choice); (ii) they switch to other cleaners (partner switching); and (iii) they aggressively chase uncooperative cleaners (punishment) [63,64]. After such punishment, cleaner fish act more cooperatively and are less likely to feed on mucus [63,64].…”

Punish or perish? Retaliation and collaboration among humans

“…Punishment is not the only way to enforce cooperation; harassing those having access to a resource [67], chasing shirkers [68] or sabotaging the attempts of cheaters [16], are different examples, and can also be found in other animals, such as mammals, fishes or insects. But humans, with their cognitive capacities for individual recognition, temporal discounting, memory, empathy and language, are uniquely gifted to develop the proximal mechanisms needed for reciprocation and in particular for punishment.…”

Do cleaner fish learn to feed against their preference in a reverse reward contingency task?

“…Therefore, they needed to swim away from the more attractive item and approach the less attractive item in order to solve the task. This subtle but perhaps important diVerence might explain why cleaners largely failed in the reverse reward contingency task, while they can easily learn to feed on a non preferred food item from a plate when a preferred item is present on the same plate in 1 cm distance (Bshary and Grutter 2005;Bshary and Grutter 2006). In these earlier experiments, each subject was allowed to continue to feed on a plate with two types of food as long as it continued to feed on the non-preferred item (Xakes).…”

“…We predicted that cleaners should be able to solve a reverse reward contingency task, based on the fact that cleaners can control impulsive behaviour in a diVerent situation, i.e. when they feed against their preference in interactions with client reef Wsh (Grutter and Bshary 2003;Bshary and Grutter 2005;Bshary et al 2007;.…”

“…biting) cleaners by leaving the cleaning station or attacking (punishing) the cleaner (Bshary and Grutter 2002a;Bshary and SchäVer 2002), cleaners adjust their behaviour and feed on the parasites they obtain from clients (Grutter 1996;Bshary and Grutter 2002b). Several laboratory experiments show that cleaners can easily learn to feed against their preference if this allows them to continue with foraging (Bshary and Grutter 2005;Bshary and Grutter 2006). This foraging behaviour results in a cooperative interaction under natural conditions.…”