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 m(2) 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 m(2) 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. (C) 2018 Elsevier B.V. All rights reserved

Macroalgae removal on coral reefs: realised ecosystem functions transcend biogeographic locations

Coral reef ecosystems are at the forefront of biodiversity loss and climate change-mediated transformations. This is expected to have profound consequences for the functioning of these ecosystems. However, assessments of ecosystem function on reefs are often spatially limited, within biogeographic realms, or rely on presumed proxies such as traits. To address these shortcomings and assess the effects of biogeography and fish presence on the critical ecosystem function of macroalgal removal, we used assays of six algal genera across three reef habitats in two biogeographically distinct locations: Little Cayman in the Caribbean and Lizard Island on the Great Barrier Reef (GBR). Patterns of fish feeding and realised ecosystem function were strikingly similar between the two geographic locations, despite a threefold difference in the local diversity of nominally herbivorous fishes, a 2.4-fold difference in the diversity of fishes feeding and differences in the biogeographic history of the two locations. In both regions, a single species dominated the function: a surgeonfish, Naso unicornis, at the GBR location and, surprisingly, a triggerfish, Melichthys niger, at the Caribbean location. Both species, especially M. niger, were relatively rare, compared to other nominally herbivorous fishes, in censuses covering more than 14,000 m(2) at each location. Our study provides novel insights into the critical function of macroalgal removal in hyperdiverse coral reef ecosystems, highlighting: (a) that function can transcend biogeographic, taxonomic and historical constraints; and (b) shortcomings in our assumptions regarding fish presence and realised ecosystem function on coral reefs

Cue-based decision rules of cleaner fish in a biological market task

To develop an evolutionary theory of social decision making, we require an understanding of how individuals utilize environmental cues to form decision rules. We exposed ‘cleaner’ fish (bluestreak cleaner wrasse, Labroides dimidiatus) to a biological market task, where giving priority to an ephemeral (i.e. ‘visitor’ client) food plate, over a permanent (i.e. ‘resident’ client) plate, doubled the food reward. Previously published experiments revealed that adult cleaners from a complex social environment regularly solved this task and outperformed adult cleaners from a simple social environment as well as juveniles from both habitat types. In these studies, plates were differentiated by colour and/or colour pattern. However, client size is another potentially useful cue that may be used by cleaners to solve the biological market task in nature, as visitor clients are typically larger than resident clients. Here, we tested cleaners in a setting where plates differed only in size and not colour/pattern: the majority of cleaners exhibited a spontaneous preference for inspecting larger plates or were more likely to reach the task-solving criterion if the visitor plate was larger. All cleaners were able to solve the task when we incorporated both size and colour/pattern cues; however, only cleaners from the complex social environment settled on the more precise colour/pattern cue. In contrast, cleaners from the simple social environment relied on size as the primary, yet less precise, cue to solve the task. In conclusion, our results strongly suggest that intraspecific variation in the performance of cleaners in the biological market task is based on variation in the relative salience of available cues and correlates with variation in a cleaner's natural social environment. Variation in the relative salience of available cues may therefore explain a portion of the intra- and interspecific variance in cognitive performance and social behaviour documented in other animal species

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

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

Cross-shelf benthic community structure on the Great Barrier Reef: relationships between macroalgal cover and herbivore biomass

The Great Barrier Reef (GBR) is one of the most extensively studied coral reef systems in the world, yet to date, there has been no comprehensive multi-spatial scale evaluation of its benthic community structure. Such descriptions provide a useful reference point for evaluating future community changes. Moreover, large-scale associations between macroalgae and herbivory on the GBR are yet to be investigated. Our aim, therefore, was to quantify all major substratum categories across multiple spatial scales and investigate cross-shelf relationships between macroalgal cover and herbivore biomass. Using point-intercept transects and timed underwater censuses, individual benthic\ud components and roving herbivorous fish densities were quantified across 3 spatial scales: latitude, continental shelf position and within-reef habitat. Principal component analysis and analysis of similarities (ANOSIM) revealed a distinct separation of inner-shelf reef habitats from all mid- and outer-shelf habitats in both northern and central regions of the GBR. Macroalgal cover was generally high on inner-shelf reefs (36 to 66%) and decreased markedly on all mid- and outer-shelf habitats (0 to 15%). A significant negative correlation was found between macroalgal cover and total herbivorous fish biomass, but no relationship was found between macroalgal cover and macroalgal browser\ud biomass. In contrast to macroalgae, the cover of crustose coralline algae and live scleractinian corals increased markedly across the shelf in both regions of the GBR. These patterns appear to be shaped by both physical and biological factors, including wave energy, sedimentation and grazing intensity

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

Extreme recent weather events hitting the Great Barrier Reef, i.e., cyclones and the 2016 El Niño enabled us to explore potential consequences on marine cleaning mutualism involving the cleaner fish <i>Labroides dimidiatus</i> (hereafter ‘cleaner’), a key species for fish biodiversity on coral reefs

Biological market effects predict cleaner fish strategic sophistication

Market-like situations emerge in nature when trading partners exchange goods and services. However, how partner choice option contributes to the expression of social strategic sophistication (i.e., the ability to adjust behavior flexibly given the specifics of a situation) is still poorly understood. A suitable study system to explore this question is the "cleaner" fish Labroides dimidiatus. Cleaners trade parasite removal in exchange for food with a variety of "client" species. Previous research documented strong interindividual variation in two features of their strategic sophistication, namely, the ability to adjust service quality to the presence of an audience and to give priority to clients with access to alternative cleaners ("visitor clients") over clients lacking such choice options ("resident clients"). Here, we sampled various demes (i.e., group of individuals) of the same population of cleaner fish in order to investigate the extent to which factors describing fish densities and cleaning interaction patterns predict the strategic sophistication in two laboratory experiments. These experiments tested whether cleaners could increase their food intake through reputation management and/or learning to provide service priority to a visitor-like ephemeral food plate. We found that high "outbidding competition," characterized by high densities of cleaners and visitor clients, along with visitor's behavior promoting such competition, consistently predicted high strategic sophistication in cleaners. A better understanding of the role of learning versus potential genetic factors, interacting with local market conditions to affect strategic sophistication, is needed to clarify how natural selection has promoted the evolution and maintenance of cooperation in this cleaning mutualism