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.

Figure 1

Experimental Plexiglas plate. The stripes on the plates that are illustrated in black had two different colouration patterns, either pink and black or yellow and beige. The initial preference test was conducted with one plate type, and the teaching trials and the final experiment with the other plate type. Fourteen food items were offered in each trial. Grid cells were filled from the upper left to the lower right, according to a random, but balanced, sequence from a random table. Once one food type had been selected seven times, the remaining grid cells were filled with the other food type. Each random sequence was used only once in each of the three treatment groups; the sequence shown in the figure is just one possibility. P, prawn item (corresponding to a 0 in the random sequence); F, flake item (corresponding to a 1 in the random sequence). On the right of the plate is the lever (40 cm long) that allowed the experimenter to react to cleaner fishes' foraging behaviour according to the treatment group (no reaction, fleeing, or chasing in response to prawn feeding).

Figure 2

The percentage of prawn items eaten in the three treatment groups during the initial preference test (grey columns) and during the final experiment after the teaching period (white columns). Shown are the median and the interquartiles for n=8 individual cleaners for each treatment.