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Noise produced by anthropogenic activities is increasing in many marine ecosystems. We investigated the effect of playback of boat noise on fish cognition. We focused on noise from small motorboats, since its occurrence can dominate soundscapes in coastal communities, the number of noise-producing vessels is increasing rapidly and their proximity to marine life has the potential to cause deleterious effects. Cognition-or the ability of individuals to learn and remember information-is crucial, given that most species rely on learning to achieve fitness-promoting tasks, such as finding food, choosing mates and recognizing predators. The caveat with cognition is its latent effect: the individual that fails to learn an important piece of information will live normally until the moment where it needs the information to make a fitness-related decision. Such latent effects can easily be overlooked by traditional risk assessment methods. Here, we conducted three experiments to assess the effect of boat noise playbacks on the ability of fish to learn to recognize predation threats, using a common, conserved learning paradigm. We found that fish that were trained to recognize a novel predator while being exposed to 'reef + boat noise' playbacks failed to subsequently respond to the predator, while their 'reef noise' counterparts responded appropriately. We repeated the training, giving the fish three opportunities to learn three common reef predators, and released the fish in the wild. Those trained in the presence of 'reef + boat noise' playbacks survived 40% less than the 'reef noise' controls over our 72 h monitoring period, a performance equal to that of predator-naive fish. Our last experiment indicated that these results were likely due to failed learning, as opposed to stress effects from the sound exposure. Neither playbacks nor real boat noise affected survival in the absence of predator training. Our results indicate that boat noise has the potential to cause latent effects on learning long after the stressor has gone., (© 2018 The Author(s).)

Coral reefs are biodiversity hotpots that are under significant threat due to the degradation and death of hard corals. When obligate coral-dwelling species die, the remaining species must either move or adjust to the altered conditions. Our goal was to investigate the effect of coral degradation on the ability of coral reef fishes to assess their risk of predation using alarm cues from injured conspecifics. Here, we tested the ability of six closely related species of juvenile damselfish (Pomacentridae) to respond to risk cues in both live coral or dead-degraded coral environments. Of those six species, two are exclusively associated with live coral habitats, two are found mostly on dead-degraded coral rubble, while the last two are found in both habitat types. We found that the two live coral associates failed to respond appropriately to the cues in water from degraded habitats. In contrast, the cue response of the two rubble associates was unaffected in the same degraded habitat. Interestingly, we observed a mixed response from the species found in both habitat types, with one species displaying an appropriate cue response while the other did not. Our second experiment suggested that the lack of responses stemmed from deactivation of the alarm cues, rather than the inability of the species to smell. Habitat preference (live coral versus dead coral associates) and phylogeny are good candidates for future work aimed at predicting which species are affected by coral degradation. Our results point towards a surprising level of variation in the ability of congeneric species to fare in altered habitats and hence underscores the difficulty of predicting community change in degraded habitats., (© 2017 The Authors.)

Many vertebrates are known to show behavioural lateralization, whereby they differentially use one side of their body or either of their bilateral organs or limbs. Behavioural lateralization often manifests in a turning bias in fishes, with some individuals showing a left bias and others a right bias. Such biases could be the source of considerable conflict in fish schools given that there may be considerable social pressure to conform to the group to maintain effective group evasion. Here, we show that predation pressure is a major determinant of the degree of lateralization, both in a relative and absolute sense, in yellow-and-blueback fusiliers (Caesio teres), a schooling fish common on coral reefs. Wild-caught fish showed a bias for right turning. When predation pressure was experimentally elevated or relaxed, the strength of lateralization changed. Higher predation pressure resulted in an increase in the strength of lateralization. Individuals that exhibited the same turning bias as the majority of individuals in their group had improved escape performance compared with individuals that were at odds with the group. Moreover, individuals that were right-biased had improved escape performance, compared with left-biased ones. Plasticity in lateralization might be an important evolutionary consequence of the way gregarious species respond to predators owing to the probable costs associated with this behaviour., (© 2016 The Author(s).)

Noise-generating human activities affect hearing, communication and movement in terrestrial and aquatic animals, but direct evidence for impacts on survival is rare. We examined effects of motorboat noise on post-settlement survival and physiology of a prey fish species and its performance when exposed to predators. Both playback of motorboat noise and direct disturbance by motorboats elevated metabolic rate in Ambon damselfish (Pomacentrus amboinensis), which when stressed by motorboat noise responded less often and less rapidly to simulated predatory strikes. Prey were captured more readily by their natural predator (dusky dottyback, Pseudochromis fuscus) during exposure to motorboat noise compared with ambient conditions, and more than twice as many prey were consumed by the predator in field experiments when motorboats were passing. Our study suggests that a common source of noise in the marine environment has the potential to impact fish demography, highlighting the need to include anthropogenic noise in management plans.

Habitat degradation is one of the 'Big Five' drivers of biodiversity loss. However, the mechanisms responsible for this progressive loss of biodiversity are poorly understood. In marine ecosystems, corals play the role of ecosystem engineers, providing essential habitat for hundreds of thousands of species and hence their health is crucial to the stability of the whole ecosystem. Climate change is causing coral bleaching and degradation, and while this has been known for a while, little do we know about the cascading consequences of these events on the complex interrelationships between predators and their prey. The goal of our study was to investigate, under completely natural conditions, the effect of coral degradation on predator-prey interactions. Settlement stage ambon damselfish (Pomacentrus amboinensis), a common tropical fish, were released on patches of healthy or dead corals, and their behaviours in situ were measured, along with their response to injured conspecific cues, a common risk indicator. This study also explored the effect of habitat degradation on natural levels of mortality at a critical life-history transition. We found that juveniles in dead corals displayed risk-prone behaviours, sitting further away and higher up on the reef patch, and failed to respond to predation cues, compared to those on live coral patches. In addition, in situ survival experiments over 48 h indicated that juveniles on dead coral habitats had a 75% increase in predation-related mortality, compared to fish released on live, healthy coral habitats. Our results provide the first of many potential mechanisms through which habitat degradation can impact the relationship between prey and predators in the coral reef ecosystem. As the proportion of dead coral increases, the recruitment and replenishment of coral reef fishes will be threatened, and so will the level of diversity in these biodiversity hot spots., (© 2014 The Authors. Journal of Animal Ecology © 2014 British Ecological Society.)

Much of the plasticity that prey exhibit in response to predators is linked to the prey's immediate background level of risk. However, we know almost nothing of how background risk influences how prey learn to categorize predators and non-predators. Learning non-predators probably represents one of the most underappreciated aspects of anti-predator decision-making. Here, we provide larval damselfish (Pomacentrus chrysurus) with a high or low background risk and then try to teach them to recognize a cue as non-threatening through the process of latent inhibition. Prey from the low-risk background that were pre-exposed to the novel odour cues in the absence of negative reinforcement for 3 days, and then provided the opportunity to learn to recognize the odour as threatening, failed to subsequently respond to the odour as a threat. Fish from the high-risk background showed a much different response. These fish did not learn the odour as non-threatening, probably because the cost of falsely learning an odour as non-threatening is higher when the background level of risk is higher. Our work highlights that background level of risk appears to drive plasticity in cognition of prey animals learning to discriminate threats in their environment., (© 2014 The Author(s) Published by the Royal Society. All rights reserved.)

Despite considerable study, mystery surrounds the use of signals that initiate cooperative hunting in animals. Using a labyrinth test chamber, we examined whether a lionfish, Dendrochirus zebra, would initiate cooperative hunts with piscine partners. We found that D. zebra uses a stereotyped flared fin display to alert conspecific and heterospecific lionfish species Pterois antennata to the presence of prey. Per capita success rate was significantly higher for cooperative hunters when compared with solitary ones, with hunt responders assisting hunt initiators in cornering the prey using their large extended pectoral fins. The initiators would most often take the first strike at the group of prey, but both hunters would then alternate striking at the remaining prey. Results suggest that the cooperative communication signal may be characteristic to the lionfish family, as interspecific hunters were equally coordinated and successful as intraspecific hunters. Our findings emphasize the complexity of collaborative foraging behaviours in lionfish; the turn-taking in strikes suggests that individuals do not solely try to maximize their own hunting success: instead they equally share the resources between themselves. Communicative group hunting has enabled Pteroine fish to function as highly efficient predators., (© 2014 The Author(s) Published by the Royal Society. All rights reserved.)

The ability of prey to observe and learn to recognize potential predators from the behaviour of nearby individuals can dramatically increase survival and, not surprisingly, is widespread across animal taxa. A range of sensory modalities are available for this learning, with visual and chemical cues being well-established modes of transmission in aquatic systems. The use of other sensory cues in mediating social learning in fishes, including mechano-sensory cues, remains unexplored. Here, we examine the role of different sensory cues in social learning of predator recognition, using juvenile damselfish (Amphiprion percula). Specifically, we show that a predator-naive observer can socially learn to recognize a novel predator when paired with a predator-experienced conspecific in total darkness. Furthermore, this study demonstrates that when threatened, individuals release chemical cues (known as disturbance cues) into the water. These cues induce an anti-predator response in nearby individuals; however, they do not facilitate learnt recognition of the predator. As such, another sensory modality, probably mechano-sensory in origin, is responsible for information transfer in the dark. This study highlights the diversity of sensory cues used by coral reef fishes in a social learning context.

The ability of prey to recognize predators is a fundamental prerequisite to avoid being eaten. Indeed, many prey animals learn to distinguish species that pose a threat from those that do not. Once the prey has learned the identity of one predator, it may generalize this recognition to similar predators with which the prey has no experience. The ability to generalize reduces the costs associated with learning and further enhances the ability of the prey to avoid relevant threats. For many aquatic organisms, recognition of predators is based on odor signatures, consequently any anthropogenic alteration in water chemistry has the potential to impair recognition and learning of predators. Here we explored whether episodic acidification could influence the ability of juvenile rainbow trout to learn to recognize an unknown predator and then generalize this recognition to a closely related predator. Trout were conditioned to recognize the odor of pumpkinseed sunfish under circumneutral (~pH 7) conditions, and then tested for recognition of pumpkinseed or longear sunfish under both neutral or weakly acidic (~pH 6) conditions. When tested for a response to pumpkinseed odor, we found no significant effect of predator odor pH: trout responded similarly regardless of pH. Moreover, under neutral conditions, trout were able to generalize their recognition to the odor of longear sunfish. However, the trout could not generalize their recognition of the longear sunfish under acidic conditions. Given the widespread occurrence of anthropogenic acidification, acid-mediated impairment of predator recognition and generalization may be a pervasive problem for freshwater salmonid populations and other aquatic organisms., (Copyright © 2012 Elsevier B.V. All rights reserved.)

Predators use a variety of information sources to locate potential prey, and likewise prey animals use numerous sources of information to detect and avoid becoming the meal of a potential predator. In freshwater environments, chemosensory cues often play a crucial role in such predator/prey interactions. The importance of chemosensory information to teleost fish in marine environments is not well understood. Here, we tested whether coral reef fish predators are attracted to damage-released chemical cues from already wounded prey in order to find patches of prey and minimize their own costs of obtaining food. Furthermore, we tested if these chemical cues would convey information about status of the prey. Using y-maze experiments, we found that predatory dottybacks, Pseudochromis fuscus, were more attracted to skin extracts of damselfish, Pomacentrus amboinensis, prey that were in good condition compared to prey in poor body condition. Moreover, in both the laboratory and field, we found that predators could differentiate between skin extracts from prey based on prey size, showing a greater attraction to extracts made from prey that were the appropriate size to consume. This suggests that predators are not attracted to any general substance released from an injured prey fish instead being capable of detecting and distinguishing relatively small differences in the chemical composition of the skin of their prey. These results have implications for understanding predator foraging strategies and highlights that chemical cues play a complex role in predator-prey interactions in marine fish.

Many fishes possess specialized epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fishes. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water moulds: Saprolegnia ferax and Saprolegnia parasitica), skin-penetrating parasites (larval trematodes: Teleorchis sp. and Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fishes challenged with Saprolegnia. These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialized cells arose and are maintained by natural selection owing to selfish benefits unrelated to predator-prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation.