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
naïve 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.
Naïve 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 1 to 5 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 demonstrate 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 naïve individuals
of native species.