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Coral reefs are degrading globally due to increased environmental stressors including warming and elevated levels of pollutants. These stressors affect not only habitat-forming organisms, such as corals, but they may also directly affect the organisms that inhabit these ecosystems. Here, we explore how the dual threat of habitat degradation and microplastic exposure may affect the behaviour and survival of coral reef fish in the field. Fish were caught prior to settlement and pulse-fed polystyrene microplastics six times over 4 days, then placed in the field on live or dead-degraded coral patches. Exposure to microplastics or dead coral led fish to be bolder, more active and stray further from shelter compared to control fish. Effect sizes indicated that plastic exposure had a greater effect on behaviour than degraded habitat, and we found no evidence of synergistic effects. This pattern was also displayed in their survival in the field. Our results highlight that attaining low concentrations of microplastic in the environment will be a useful management strategy, since minimizing microplastic intake by fishes may work concurrently with reef restoration strategies to enhance the resilience of coral reef populations.

Habitat degradation is a key factor leading to the global loss of biodiversity. This problem is particularly acute in coral reef ecosystems. We investigated whether recognition of predator odours by damselfish was influenced by coral degradation and whether these changes altered survival in the wild. We taught whitespot damselfish to recognize the odour of a predator in the presence of live/healthy coral or dead/degraded coral. Fish were tested for a response to predator odours in environments that matched their conditioning environment or in environments that were mismatched. Next, we taught blue damselfish to recognize the odour of three common reef predators in live and degraded coral environments and then stocked them onto live or degraded patch reefs, where we monitored their subsequent response to predator odour along with their survival. Damselfish learned to recognize predator odours in both coral environments, but the intensity of their antipredator response was much greater when the conditioning and test environments matched. Fish released on degraded coral had about 50% higher survival if they had been trained in the presence of degraded coral rather than live coral. Altering the intensity of antipredator responses could have rather profound consequences on population growth.

Oceans of the future are predicted to be more acidic and noisier, particularly along the productive coastal fringe. This study examined the independent and combined effects of short-term exposure to elevated CO 2 and boat noise on the predator-prey interactions of a pair of common coral reef fishes ( Pomacentrus wardi and its predator, Pseudochromis fuscus ). Successful capture of prey by predators was the same regardless of whether the pairs had been exposed to ambient control conditions, the addition of either playback of boat noise, elevated CO 2 (925 µatm) or both stressors simultaneously. The kinematics of the interaction were the same for all stressor combinations and differed from the controls. The effects of CO 2 or boat noise were the same, suggesting that their effects were substitutive in this situation. Prey reduced their perception of threat under both stressors individually and when combined, and this coincided with reduced predator attack distances and attack speeds. The lack of an additive or multiplicative effect when both stressors co-occurred was notable given the different mechanisms involved in sensory disruptions and highlights the importance of determining the combined effects of key drivers to aid in predicting community dynamics under future environmental scenarios., (© 2018 The Author(s).)

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).)

Ocean acidification and warming, driven by anthropogenic CO 2 emissions, are considered to be among the greatest threats facing marine organisms. While each stressor in isolation has been studied extensively, there has been less focus on their combined effects, which could impact key ecological processes. We tested the independent and combined effects of short-term exposure to elevated CO 2 and temperature on the predator-prey interactions of a common pair of coral reef fishes ( Pomacentrus wardi and its predator, Pseudochromis fuscus ). We found that predator success increased following independent exposure to high temperature and elevated CO 2 Overall, high temperature had an overwhelming effect on the escape behaviour of the prey compared with the combined exposure to elevated CO 2 and high temperature or the independent effect of elevated CO 2 Exposure to high temperatures led to an increase in attack and predation rates. By contrast, we observed little influence of elevated CO 2 on the behaviour of the predator, suggesting that the attack behaviour of P. fuscus was robust to this environmental change. This is the first study to address how the kinematics and swimming performance at the basis of predator-prey interactions may change in response to concurrent exposure to elevated CO 2 and high temperatures and represents an important step to forecasting the responses of interacting species to climate change., (© 2017 The Author(s).)

Anthropogenic noise is a pollutant of international concern, with mounting evidence of disturbance and impacts on animal behaviour and physiology. However, empirical studies measuring survival consequences are rare. We use a field experiment to investigate how repeated motorboat-noise playback affects parental behaviour and offspring survival in the spiny chromis ( Acanthochromis polyacanthus ), a brooding coral reef fish. Repeated observations were made for 12 days at 38 natural nests with broods of young. Exposure to motorboat-noise playback compared to ambient-sound playback increased defensive acts, and reduced both feeding and offspring interactions by brood-guarding males. Anthropogenic noise did not affect the growth of developing offspring, but reduced the likelihood of offspring survival; while offspring survived at all 19 nests exposed to ambient-sound playback, six of the 19 nests exposed to motorboat-noise playback suffered complete brood mortality. Our study, providing field-based experimental evidence of the consequences of anthropogenic noise, suggests potential fitness consequences of this global pollutant., (© 2017 The Authors.)

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).)

Habitat degradation is a global problem and one of the main causes of biodiversity loss. Though widespread, the mechanisms that underlie faunal changes are poorly understood. In tropical marine systems, corals play a crucial role in forming habitat, but coral cover on many reefs is declining sharply. Coral degradation affects the olfactory cues that provide reliable information on the presence and intensity of threat. Here, we show for the first time that the ability of a habitat generalist to learn predators using an efficient and widespread method of predator learning is compromised in degraded coral habitats. Results indicate that chemical alarm cues are no longer indicative of a local threat for the habitat generalist (the damselfish, Pomacentrus amboinensis), and these cues can no longer be used to learn the identity of novel predators in degraded habitats. By contrast, a rubble specialist and congeneric (Pomacentrus coelestis) responded to olfactory threat cues regardless of background environment and could learn the identity of a novel predator using chemical alarm cues. Understanding how some species can cope with or acclimate to the detrimental impacts of habitat degradation on risk assessment abilities will be crucial to defining the scope of resilience in threatened communities., (© 2016 The Author(s).)

In aquatic environments, many prey animals possess damage-released chemical alarm cues that elicit antipredator behaviours in responsive con- and heterospecifics. Despite considerable study, the selective advantage of alarm cues remains unclear. In an attempt to investigate one of the more promising hypotheses concerning the evolution of alarm cues, we examined whether the cue functions in a fashion analogous to the distress vocalizations emitted by many terrestrial animals. Our results suggest that chemical alarm cues in damselfish (Pomacentridae) may have evolved to benefit the cue sender by attracting secondary predators who disrupt the predation event, allowing the prey a greater chance to escape. The coral reef piscivore, the dusky dottyback (Pseudochromis fuscus), chemically eavesdrops on predation events and uses chemical alarm cues from fish prey (lemon damselfish; Pomacentrus moluccensis) in an attempt to find and steal prey from primary predators. Field studies showed that Ps. fuscus aggregate at sites where prey alarm cue has been experimentally released. Furthermore, secondary predators attempted to steal captured prey of primary predators in laboratory trials and enhanced prey escape chances by 35-40%. These results are the first, to the best of our knowledge, to demonstrate a mechanism by which marine fish may benefit from the production and release of alarm cues, and highlight the complex and important role that semiochemicals play in marine predator-prey interactions., (© 2015 The Author(s).)

Neophobia--the generalized fear response to novel stimuli--provides the first potential strategy that predator-naive prey may use to survive initial predator encounters. This phenotype appears to be highly plastic and present in individuals experiencing high-risk environments, but rarer in those experiencing low-risk environments. Despite the appeal of this strategy as a 'solution' for prey naivety, we lack evidence that this strategy provides any fitness benefit to prey. Here, we compare the relative effect of environmental risk (high versus low) and predator-recognition training (predator-naive versus predator-experienced individuals) on the survival of juvenile fish in the wild. We found that juveniles raised in high-risk conditions survived better than those raised in low-risk conditions, providing the first empirical evidence that environmental risk, in the absence of any predator-specific information, affects the way naive prey survive in a novel environment. Both risk level and experience affected survival; however, the two factors did not interact, indicating that the information provided by both factors did not interfere or enhance each other. From a mechanistic viewpoint, this indicates that the combination of the two factors may increase the intensity, and hence efficacy, of prey evasion strategies, or that both factors provide qualitatively separate benefits that would result in an additive survival success.

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.)

Rising CO2 levels in the oceans are predicted to have serious consequences for many marine taxa. Recent studies suggest that non-genetic parental effects may reduce the impact of high CO2 on the growth, survival and routine metabolic rate of marine fishes, but whether the parental environment mitigates behavioural and sensory impairment associated with high CO2 remains unknown. Here, we tested the acute effects of elevated CO2 on the escape responses of juvenile fish and whether such effects were altered by exposure of parents to increased CO2 (transgenerational acclimation). Elevated CO2 negatively affected the reactivity and locomotor performance of juvenile fish, but parental exposure to high CO2 reduced the effects in some traits, indicating the potential for acclimation of behavioural impairment across generations. However, acclimation was not complete in some traits, and absent in others, suggesting that transgenerational acclimation does not completely compensate the effects of high CO2 on escape responses.

Ocean acidification poses a range of threats to marine invertebrates; however, the potential effects of rising carbon dioxide (CO2) on marine invertebrate behaviour are largely unknown. Marine gastropod conch snails have a modified foot and operculum allowing them to leap backwards rapidly when faced with a predator, such as a venomous cone shell. Here, we show that projected near-future seawater CO2 levels (961 µatm) impair this escape behaviour during a predator-prey interaction. Elevated-CO2 halved the number of snails that jumped from the predator, increased their latency to jump and altered their escape trajectory. Physical ability to jump was not affected by elevated-CO2 indicating instead that decision-making was impaired. Antipredator behaviour was fully restored by treatment with gabazine, a GABA antagonist of some invertebrate nervous systems, indicating potential interference of neurotransmitter receptor function by elevated-CO2, as previously observed in marine fishes. Altered behaviour of marine invertebrates at projected future CO2 levels could have potentially far-reaching implications for marine ecosystems.

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.

Coral bleaching has caused catastrophic changes to coral reef ecosystems around the world with profound ecological, social and economic repercussions. While its occurrence is predicted to increase in the future, we have little understanding of mechanisms that underlie changes in the fish community associated with coral degradation. The present study uses a field-based experiment to examine how the intensity of interference competition between juveniles of two species of damselfish changes as healthy corals degrade through thermal bleaching. The mortality of a damselfish that is a live coral specialist (Pomacentrus moluccensis) increased on bleached and dead coral in the presence of the habitat generalist (Pomacentrus amboinensis). Increased mortality of the specialist was indirectly owing to enhanced aggression by the generalist forcing the specialist higher up and further away from shelter on bleached and dead coral. Evidence from this study stresses the importance of changing interspecific interactions to community dynamics as habitats change.

Determining how prey learn the identity of predators and match their vigilance with current levels of threat is central to understanding the dynamics of predator-prey systems and the determinants of fitness. Our study explores how feeding history influences the relative importance of olfactory and visual sensory modes of learning, and how the experience gained through these sensory modes influences behaviour and survival in the field for a juvenile coral reef damselfish. We collected young fish immediately prior to their settlement to benthic habitats. In the laboratory, these predator-naïve fish were exposed to a high- or low-food ration and then conditioned to recognize the olfactory cues (odours) and/or visual cues from two common benthic predators. Fish were then allowed to settle on reefs in the field, and their behaviour and survival over 70 h were recorded. Feeding history strongly influenced their willingness to take risks in the natural environment. Conditioning in the laboratory with visual, olfactory or both cues from predators led fish in the field to display risk-averse behaviour compared with fish conditioned with sea water alone. Well-fed fish that were conditioned with visual, chemical or a combination of predator cues survived eight times better over the first 48 h on reefs than those with no experience of benthic predator cues. This experiment highlights the importance of a flexible and rapid mechanism of learning the identity of predators for survival of young fish during the critical life-history transition between pelagic and benthic habitats.

In 1950, Rensch noted that in clades where males are the larger sex, sexual size dimorphism (SSD) tends to be more pronounced in larger species. This fundamental allometric relationship is now known as 'Rensch's rule'. While most researchers attribute Rensch's rule to sexual selection for male size, experimental evidence is lacking. Here, we suggest that ultimate hypotheses for Rensch's rule should also apply to groups of individuals and that individual trait plasticity can be used to test those hypotheses experimentally. Specifically, we show that in the sex-changing fish Parapercis cylindrica, larger males have larger harems with larger females, and that SSD increases with harem size. Thus, sexual selection for male body size is the ultimate cause of sexual size allometry. In addition, we experimentally illustrate a positive relationship between polygyny potential and individual growth rate during sex change from female to male. Thus, sexual selection is the ultimate cause of variation in growth rate, and variation in growth rate is the proximate cause of sexual size allometry. Taken together, our results provide compelling evidence in support of the sexual selection hypothesis for Rensch's rule and highlight the potential importance of individual growth modification in the shaping of morphological patterns in Nature.

For organisms with complex life cycles, variation among individuals in traits associated with survival in one life-history stage can strongly affect the performance in subsequent stages with important repercussions on population dynamics. To identify which individual attributes are the most influential in determining patterns of survival in a cohort of reef fish, we compared the characteristics of Pomacentrus amboinensis surviving early juvenile stages on the reef with those of the cohort from which they originated. Individuals were collected at hatching, the end of the planktonic phase, and two, three, four, six and eight weeks post-settlement. Information stored in the otoliths of individual fish revealed strong carry-over effects of larval condition at hatching on juvenile survival, weeks after settlement (i.e. smaller-is-better). Among the traits examined, planktonic growth history was, by far, the most influential and long-lasting trait associated with juvenile persistence in reef habitats. However, otolith increments suggested that larval growth rate may not be maintained during early juvenile life, when selective mortality swiftly reverses its direction. These changes in selective pressure may mediate growth-mortality trade-offs between predation and starvation risks during early juvenile life. Ontogenetic changes in the shape of selectivity may be a mechanism maintaining phenotypic variation in growth rate and size within a population.