A decrease in the abundance and strategic sophistication of cleaner fish after environmental perturbations.

Coral reef ecosystems are declining worldwide and under foreseeable threat due to climate change, resulting in significant changes in reef communities. It is unknown, however, how such community changes impact interspecific interactions. Recent extreme weather events affecting the Great Barrier Reef, that is, consecutive cyclones and the 2016 El Niño event, allowed us to explore potential consequences in the mutualistic interactions involving cleaner fish Labroides dimidiatus (hereafter "cleaner"). After the perturbations, cleaner densities were reduced by 80%, disproportionally compared to the variety of reef fish clients from which cleaners remove ectoparasites. Consequently, shifts in supply and demand yielded an increase in the clients' demand for cleaning. Therefore, clients became less selective toward cleaners, whereas cleaners were able to choose from a multitude of partners. In parallel, we found a significant decline in the ability of cleaners to manage their reputation and to learn to prioritize ephemeral food sources to maximize food intake in laboratory experiments. In other words, cleaners failed to display the previously documented strategic sophistication that made this species a prime example for fish intelligence. In conclusion, low population densities may cause various effects on individual behavior, and as a consequence, interspecific interactions. At the same time, our data suggest that a recovery of population densities would cause a recovery of previously described interaction patterns and cleaner strategic sophistication within the lifetime of individuals.

Generalized rule application in bluestreak cleaner wrasse (Labroides dimidiatus): using predator species as social tools to reduce punishment.

Generalized rule application promotes flexible behavior by allowing individuals to adjust quickly to environmental changes through generalization of previous learning. Here, we show that bluestreak 'cleaner' wrasse (Labroides dimidiatus) uses generalized rule application in their use of predators as social tools against punishing reef fish clients. Punishment occurs as cleaners do not only remove ectoparasites from clients, but prefer to feed on client mucus (constituting cheating). We tested for generalized rule application in a series of experiments, starting by training cleaners to approach one of two fish models in order to evade punishment (by chasing) from a 'cheated' client model. Cleaners learned this task only if the safe haven was a predator model. During consecutive exposure to pairs of novel species, including exotic models, cleaners demonstrated generalization of the 'predators-are-safe-havens' rule by rapidly satisfying learning criteria. However, cleaners were not able to generalize to a 'one-of-two-stimuli-presents-a-safe-haven' rule, as they failed to solve the task when confronted with either two harmless fish models or two predator models. Our results emphasize the importance of ecologically relevant experiments to uncover complex cognitive processes in non-human animals, like generalized rule learning in the context of social tool use in a fish.

Male cleaner wrasses adjust punishment of female partners according to the stakes.

Punishment is an important deterrent against cheating in cooperative interactions. In humans, the severity of cheating affects the strength of punishment which, in turn, affects the punished individual's future behaviour. Here, we show such flexible adjustments for the first time in a non-human species, the cleaner wrasse (Labroides dimidiatus), where males are known to punish female partners. We exposed pairs of cleaners to a model client offering two types of food, preferred 'prawn' items and less-preferred 'flake' items. Analogous to interactions with real clients, eating a preferred prawn item ('cheating') led to model client removal. We varied the extent to which female cheating caused pay-off reduction to the male and measured the corresponding severity of male punishment. Males punished females more severely when females cheated during interactions with high value, rather than low value, model clients; and when females were similar in size to the male. This pattern may arise because, in this protogynous hermaphrodite, cheating by similar-sized females may reduce size differences to the extent that females change sex and become reproductive competitors. In response to more severe punishment from males, females behaved more cooperatively. Our results show that punishment can be adjusted to circumstances and that such subtleties can have an important bearing on the outcome of cooperative interactions.

Young fishes persist despite coral loss on the Great Barrier Reef.

Unprecedented global bleaching events have led to extensive loss of corals. This is expected to lead to extensive losses of obligate coral-dependent fishes. Here, we use a novel, spatially-matched census approach to examine the nature of fish-coral dependency across two mass coral bleaching events. Despite a >40% loss of coral cover, and the ecological extinction of functionally important habitat-providing Acropora corals, we show that populations of obligate coral-dependent fishes, including Pomacentrus moluccensis, persisted and - critically - recruitment was maintained. Fishes used a wide range of alternate reef habitats, including other coral genera and dead coral substrata. Labile habitat associations of 'obligate' coral-dependent fishes suggest that recruitment may be sustained on future reefs that lack Acropora, following devastating climatic disturbances. This persistence without Acropora corals offers grounds for cautious optimism; for coral-dwelling fishes, corals may be a preferred habitat, not an obligate requirement.

Spatial mismatch in fish and coral loss following 2016 mass coral bleaching.

Record-breaking temperatures between 2015 and 2016 led to unprecedented pan-tropical bleaching of scleractinian corals. On the Great Barrier Reef (GBR), the effects were most pronounced in the remote, northern region, where over 90% of reefs exhibited bleaching. Mass bleaching that results in widespread coral mortality represents a major disturbance event for reef organisms, including reef fishes. Using 133 replicate 1 m2 quadrats, we quantified short-term changes in coral communities and spatially associated reef fish assemblages, at Lizard Island, Australia, in response to the 2016 mass bleaching event. Quadrats were spatially matched, permitting repeated sampling of fish and corals in the same areas: before, during and 6 months after mass bleaching. As expected, we documented a significant decrease in live coral cover. Subsequent decreases in fish abundance were primarily driven by coral-associated damselfishes. However, these losses, were relatively minor (37% decrease), especially compared to the magnitude of Acropora loss (>95% relative decrease). Furthermore, at a local, 1 m2 scale, we documented a strong spatial mismatch between fish and coral loss. Post-bleaching fish losses were not highest in quadrats that experienced the greatest loss of live coral. Nor were fish losses associated with a proliferation of cyanobacteria. Several sites did, however, exhibit increases in fish abundance suggesting substantial spatial movements. These results challenge common assumptions and emphasize the need for caution when ascribing causality to observed patterns of fish loss at larger spatial scales. Our results highlight the potential for short-term resilience to climate change, in fishes, through local migration and habitat plasticity.

The performance of cleaner wrasse, Labroides dimidiatus, in a reversal learning task varies across experimental paradigms.

Testing performance in controlled laboratory experiments is a powerful tool for understanding the extent and evolution of cognitive abilities in non-human animals. However, cognitive testing is prone to a number of potential biases, which, if unnoticed or unaccounted for, may affect the conclusions drawn. We examined whether slight modifications to the experimental procedure and apparatus used in a spatial task and reversal learning task affected performance outcomes in the bluestreak cleaner wrasse, Labroides dimidiatus (hereafter "cleaners"). Using two-alternative forced-choice tests, fish had to learn to associate a food reward with a side (left or right) in their holding aquarium. Individuals were tested in one of four experimental treatments that differed slightly in procedure and/or physical set-up. Cleaners from all four treatment groups were equally able to solve the initial spatial task. However, groups differed in their ability to solve the reversal learning task: no individuals solved the reversal task when tested in small tanks with a transparent partition separating the two options, whereas over 50% of individuals solved the task when performed in a larger tank, or with an opaque partition. These results clearly show that seemingly insignificant details to the experimental set-up matter when testing performance in a spatial task and might significantly influence the outcome of experiments. These results echo previous calls for researchers to exercise caution when designing methodologies for cognition tasks to avoid misinterpretations.

Reputation management promotes strategic adjustment of service quality in cleaner wrasse.

Adjusting one's behaviour in response to eavesdropping bystanders is considered a sophisticated social strategy, yet the underlying mechanisms are not well studied. Cleaner wrasse, Labroides dimidiatus, cooperate by eating ectoparasites off "client" fishes, or cheat (i.e. bite) and eat client mucus. Image scoring by bystander clients generally causes cleaners from socially-complex (i.e. high cleaner and client abundance; high client species richness) habitats to increase levels of cooperation. However, some individuals may periodically provide tactile stimulation to small resident clients, which attract bystanders close that are bitten, a form of tactical deception. Cortisol injection can reproduce this pattern. Here, we tested whether cleaners from socially-complex versus simple habitats respond differently to cortisol injections in terms of their cleaning interactions with clients. We found that only cleaners from the socially-complex habitat respond to cortisol injection with strategies functioning as tactical deception: i.e. increased tactile stimulation to small clients and increased cheating of large clients relative to small ones. At the socially-simple site, where reputation management is less important, cortisol-treated fish increased their overall levels of cheating, especially of small clients. Thus, strategic adjustments to cooperative behaviour and tactical deception are likely context-dependent, forming part of general reputation management abilities in cleaner wrasse.

Temporal comparison and predictors of fish species abundance and richness on undisturbed coral reef patches.

Large disturbances can cause rapid degradation of coral reef communities, but what baseline changes in species assemblages occur on undisturbed reefs through time? We surveyed live coral cover, reef fish abundance and fish species richness in 1997 and again in 2007 on 47 fringing patch reefs of varying size and depth at Mersa Bareika, Ras Mohammed National Park, Egypt. No major human or natural disturbance event occurred between these two survey periods in this remote protected area. In the absence of large disturbances, we found that live coral cover, reef fish abundance and fish species richness did not differ in 1997 compared to 2007. Fish abundance and species richness on patches was largely related to the presence of shelters (caves and/or holes), live coral cover and patch size (volume). The presence of the ectoparasite-eating cleaner wrasse, Labroides dimidiatus, was also positively related to fish species richness. Our results underscore the importance of physical reef characteristics, such as patch size and shelter availability, in addition to biotic characteristics, such as live coral cover and cleaner wrasse abundance, in supporting reef fish species richness and abundance through time in a relatively undisturbed and understudied region.

Adult cleaner wrasse outperform capuchin monkeys, chimpanzees and orang-utans in a complex foraging task derived from cleaner--client reef fish cooperation.

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.