Differential learning by native versus invasive predators to avoid distasteful cleaning mutualists

1. Cleaning symbioses on coral reefs are mutually beneficial interactions between two individuals, in which a 'cleaner' removes and eats parasites from the surface of a 'client' fish. A suite of behavioural and morphological traits of cleaners signal cooperation with co-evolved species, thus protecting the cleaner from being eaten by otherwise predatory clients. However, it is unclear whether cooperation between cleaners and predatory clients is innate or learned, and therefore whether an introduced predator might consume, cooperate with or alter the behaviour of cleaners. 2. We explored the role of learning in cleaning symbioses by comparing the interactions of native cleaner fishes with both naive and experienced, non-native and native fish predators. In so doing, we tested the vulnerability of the predominant cleaners on Atlantic coral reefs, cleaning gobies (Elacatinus spp.), to the recent introduction of a generalist predator, the Indo-Pacific red lionfish (Pterois volitans). 3. Naive juveniles of both invasive (P. volitans) and native predators (Cephalopholis spp. groupers) initially attacked cleaning gobies and hyperventilated from a putative toxin on the gobies' skin during laboratory experiments. After one to five such encounters, invasive lionfish often approached the cleaner closely, then turned away without striking. Consistent with learned avoidance, invasive lionfish rarely interacted with cleaning gobies in the wild, either antagonistically or cooperatively, and did not affect gobies' abundance. Native predators showed little evidence of learning during early encounters; they repeatedly attacked the cleaner during laboratory experiments and hyperventilated less violently than did lionfish. However, consistent with learned cooperation, native predators rarely antagonised and were frequently cleaned by gobies in the wild. 4. We demonstrated that rapid, learned avoidance protects a distasteful cleaning mutualist from an invasive predator. The behavioural plasticity of this invader likely contributes to its success across its invaded range. Additionally, our results suggest that the cleaner's chemical defence most likely evolved as a way to deter predation and reinforce cooperation with naive individuals of native species.

Automated summary

Cleaning symbioses on coral reefs involve mutualistic interactions between cleaner and client fish, where cleaners remove parasites from clients. The study shows that learned avoidance behavior can protect cleaners from predation by invasive predators, highlighting the importance of behavioral plasticity in mediating species interactions in marine ecosystems.