Adult Cleaner Wrasse Outperform Capuchin Monkeys, Chimpanzees and Orang-utans in a Complex Foraging Task Derived from Cleaner – Client Reef Fish Cooperation

Lucie H Salwiczek,Tara Stoinski,Lanila Demarta,Ana I Pinto,Darby Proctor,Laurent Prétôt,Jennifer Essler,Sarah F Brosnan,Sharon Wismer,Redouan Bshary

doi:10.1371/journal.pone.0049068

Abstract

The insight that animals' cognitive abilities are linked to their evolutionary history, and hence their ecology, provides the framework for the comparative approach. Despite primates renowned dietary complexity and social cognition, including cooperative abilities, we here demonstrate that cleaner wrasse outperform three primate species, capuchin monkeys, chimpanzees and orang-utans, in a foraging task involving a choice between two actions, both of which yield identical immediate rewards, but only one of which yields an additional delayed reward. The foraging task decisions involve partner choice in cleaners: they must service visiting client reef fish before resident clients to access both; otherwise the former switch to a different cleaner. Wild caught adult, but not juvenile, cleaners learned to solve the task quickly and relearned the task when it was reversed. The majority of primates failed to perform above chance after 100 trials, which is in sharp contrast to previous studies showing that primates easily learn to choose an action that yields immediate double rewards compared to an alternative action. In conclusion, the adult cleaners' ability to choose a superior action with initially neutral consequences is likely due to repeated exposure in nature, which leads to specific learned optimal foraging decision rules.

Highlights

The ecological approach to cognition proposes that a species’ ability to solve a particular problem is tightly linked to its evolutionary history and, to the ecological conditions under which it was selected [1,2,3]
The precision with which cleaners adapt current service quality to current conditions may be predicted by their ecology: cleaners have over 2000 interactions per day with a great variety of clients and fully depend on cleaning for their diet [15], their performance during the interactions has a major impact on their fitness
Initial learning tests All six adult cleaner fish individuals learned to eat first from the ephemeral plate, which was smoothly withdrawn if the cleaner were to forage on the permanent plate first

Summary

Introduction

The ecological approach to cognition proposes that a species’ ability to solve a particular problem is tightly linked to its evolutionary history and, to the ecological conditions under which it was selected [1,2,3]. The ecological approach has led to a great diversification of animals studied, and in particular to the appreciation that animal clades that lack large and complexly structured brains may provide examples of impressive cognitive abilities. This is in particular true for fishes [7], which have provided some excellent examples for complex social strategies. Male cichlids (Astatotilapia burtoni) use transitive inference to predict fighting abilities of competitors [8] and sticklebacks (Pungitius pungitius) employ so-called hill climbing social learning strategies [9], in which they compare their own foraging success with the success of observed individuals to update foraging decisions Another example involves the foraging decisions of cleaner wrasse, Labroides dimidiatus. The question of interest is whether any (vertebrate) species could behave like a cleaner wrasse if it switched its diet to ectoparasites and mucus of fishes, or whether specific selection pressures on cleaner wrasses have caused specific abilities? And if specific abilities do exist in cleaner wrasses, what is the role of cognition?

Methods

Results

Conclusion