Punishment and partner switching cause cooperative behaviour in a cleaning mutualism

TLDR

Cleaner fish and their reef fish clients cooperate when cleaners eat ectoparasites, but cleaners may cheat by eating client mucus, and clients may deter cheating through punishment or partner switching. We experimentally tested whether client punishment or partner switching elicits cooperative behaviour in cleaner fish. Cleaners were trained on Plexiglas plates offering prawn (preferred) and fish flake (non‑preferred) items, with a lever simulating client responses that punished prawn consumption but left flake consumption unpunished. After six trials, cleaners shifted markedly to flake feeding, indicating that punishment or interaction termination can override their food preference and enhance cooperative service quality.

Abstract

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.