Rapid physiological and transcriptomic changes associated with oxygen delivery in larval anemonefish suggest a role in adaptation to life on hypoxic coral reefs.

Connectivity of coral reef fish populations relies on successful dispersal of a pelagic larval phase. Pelagic larvae must exhibit high swimming abilities to overcome ocean and reef currents, but once settling onto the reef, larvae transition to endure habitats that become hypoxic at night. Therefore, coral reef fish larvae must rapidly and dramatically shift their physiology over a short period of time. Taking an integrative, physiological approach, using swimming respirometry, and examining hypoxia tolerance and transcriptomics, we show that larvae of cinnamon anemonefish (Amphiprion melanopus) rapidly transition between "physiological extremes" at the end of their larval phase. Daily measurements of swimming larval anemonefish over their entire early development show that they initially have very high mass-specific oxygen uptake rates. However, oxygen uptake rates decrease midway through the larval phase. This occurs in conjunction with a switch in haemoglobin gene expression and increased expression of myoglobin, cytoglobin, and neuroglobin, which may all contribute to the observed increase in hypoxia tolerance. Our findings indicate that critical ontogenetic changes in the gene expression of oxygen-binding proteins may underpin the physiological mechanisms needed for successful larval recruitment to reefs.

Habitat degradation negatively affects auditory settlement behavior of coral reef fishes.

Coral reefs are increasingly degraded by climate-induced bleaching and storm damage. Reef recovery relies on recruitment of young fishes for the replenishment of functionally important taxa. Acoustic cues guide the orientation, habitat selection, and settlement of many fishes, but these processes may be impaired if degradation alters reef soundscapes. Here, we report spatiotemporally matched evidence of soundscapes altered by degradation from recordings taken before and after recent severe damage on Australia's Great Barrier Reef. Postdegradation soundscapes were an average of 15 dB re 1 µPa quieter and had significantly reduced acoustic complexity, richness, and rates of invertebrate snaps compared with their predegradation equivalents. We then used these matched recordings in complementary light-trap and patch-reef experiments to assess responses of wild fish larvae under natural conditions. We show that postdegradation soundscapes were 8% less attractive to presettlement larvae and resulted in 40% less settlement of juvenile fishes than predegradation soundscapes; postdegradation soundscapes were no more attractive than open-ocean sound. However, our experimental design does not allow an estimate of how much attraction and settlement to isolated postdegradation soundscapes might change compared with isolated predegradation soundscapes. Reductions in attraction and settlement were qualitatively similar across and within all trophic guilds and taxonomic groups analyzed. These patterns may lead to declines in fish populations, exacerbating degradation. Acoustic changes might therefore trigger a feedback loop that could impair reef resilience. To understand fully the recovery potential of coral reefs, we must learn to listen.

Microplastic exposure interacts with habitat degradation to affect behaviour and survival of juvenile fish in the field.

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.

Parasite infection directly impacts escape response and stress levels in fish.

Parasites can account for a substantial proportion of the biomass in marine communities. As such, parasites play a significant ecological role in ecosystem functioning via host interactions. Unlike macropredators, such as large piscivores, micropredators, such as parasites, rarely cause direct mortality. Rather, micropredators impose an energetic tax, thus significantly affecting host physiology and behaviour via sublethal effects. Recent research suggests that infection by gnathiid isopods (Crustacea) causes significant physiological stress and increased mortality rates. However, it is unclear whether infection causes changes in the behaviours that underpin escape responses or changes in routine activity levels. Moreover, it is poorly understood whether the cost of gnathiid infection manifests as an increase in cortisol. To investigate this, we examined the effect of experimental gnathiid infection on the swimming and escape performance of a newly settled coral reef fish and whether infection led to increased cortisol levels. We found that micropredation by a single gnathiid caused fast-start escape performance and swimming behaviour to significantly decrease and cortisol levels to double. Fast-start escape performance is an important predictor of recruit survival in the wild. As such, altered fitness-related traits and short-term stress, perhaps especially during early life stages, may result in large scale changes in the number of fish that successfully recruit to adult populations.

Effect of elevated CO2 and small boat noise on the kinematics of predator-prey interactions.

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 CO2 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 CO2 (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 CO2 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.

School is out on noisy reefs: the effect of boat noise on predator learning and survival of juvenile coral reef fishes.

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.

Not equal in the face of habitat change: closely related fishes differ in their ability to use predation-related information in degraded coral.

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.

Warming has a greater effect than elevated CO2 on predator-prey interactions in coral reef fish.

Ocean acidification and warming, driven by anthropogenic CO2 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 CO2 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 CO2 Overall, high temperature had an overwhelming effect on the escape behaviour of the prey compared with the combined exposure to elevated CO2 and high temperature or the independent effect of elevated CO2 Exposure to high temperatures led to an increase in attack and predation rates. By contrast, we observed little influence of elevated CO2 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 CO2 and high temperatures and represents an important step to forecasting the responses of interacting species to climate change.

Motorboat noise impacts parental behaviour and offspring survival in a reef fish.

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.

Habitat degradation disrupts neophobia in juvenile coral reef fish.

Habitat degradation not only disrupts habitat-forming species, but alters the sensory landscape within which most species must balance behavioural activities against predation risk. Rapidly developing a cautious behavioural phenotype, a condition known as neophobia, is advantageous when entering a novel risky habitat. Many aquatic organisms rely on damage-released conspecific cues (i.e. alarm cues) as an indicator of impending danger and use them to assess general risk and develop neophobia. This study tested whether settlement-stage damselfish associated with degraded coral reef habitats were able to use alarm cues as an indicator of risk and, in turn, develop a neophobic response at the end of their larval phase. Our results indicate that fish in live coral habitats that were exposed to alarm cues developed neophobia, and, in situ, were found to be more cautious, more closely associated with their coral shelters and survived four-times better than non-neophobic control fish. In contrast, fish that settled onto degraded coral habitats did not exhibit neophobia and consequently suffered much greater mortality on the reef, regardless of their history of exposure to alarm cues. Our results show that habitat degradation alters the efficacy of alarm cues with phenotypic and survival consequences for newly settled recruits.

Disrupted learning: habitat degradation impairs crucial antipredator responses in naive prey.

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.

At odds with the group: changes in lateralization and escape performance reveal conformity and conflict in fish schools.

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.

Shoaling reduces metabolic rate in a gregarious coral reef fish species.

Many animals live in groups because of the potential benefits associated with defense and foraging. Group living may also induce a 'calming effect' on individuals, reducing overall metabolic demand. This effect could occur by minimising the need for individual vigilance and reducing stress through social buffering. However, this effect has proved difficult to quantify. We examined the effect of shoaling on metabolism and body condition in the gregarious damselfish Chromis viridis Using a novel respirometry methodology for social species, we found that the presence of shoal-mate visual and olfactory cues led to a reduction in the minimum metabolic rate of individuals. Fish held in isolation for 1 week also exhibited a reduction in body condition when compared with those held in shoals. These results indicate that social isolation as a result of environmental disturbance could have physiological consequences for gregarious species.

Top predators negate the effect of mesopredators on prey physiology.

Predation theory and empirical evidence suggest that top predators benefit the survival of resource prey through the suppression of mesopredators. However, whether such behavioural suppression can also affect the physiology of resource prey has yet to be examined. Using a three-tier reef fish food web and intermittent-flow respirometry, our study examined changes in the metabolic rate of resource prey exposed to combinations of mesopredator and top predator cues. Under experimental conditions, the mesopredator (dottyback, Pseudochromis fuscus) continuously foraged and attacked resource prey (juveniles of the damselfish Pomacentrus amboinensis) triggering an increase in prey O2 uptake by 38 ± 12·9% (mean ± SE). The visual stimulus of a top predator (coral trout, Plectropomus leopardus) restricted the foraging activity of the mesopredator, indirectly allowing resource prey to minimize stress and maintain routine O2 uptake. Although not as strong as the effect of the top predator, the sight of a large non-predator species (thicklip wrasse, Hemigymnus melapterus) also reduced the impact of the mesopredator on prey metabolic rate. We conclude that lower trophic-level species can benefit physiologically from the presence of top predators through the behavioural suppression that top predators impose on mesopredators. By minimizing the energy spent on mesopredator avoidance and the associated stress response to mesopredator attacks, prey may be able to invest more energy in foraging and growth, highlighting the importance of the indirect, non-consumptive effects of top predators in marine food webs.

Small-Boat Noise Impacts Natural Settlement Behavior of Coral Reef Fish Larvae.

After a pelagic larval phase, settlement-stage coral reef fish must locate a suitable reef habitat for juvenile life. Reef noise, produced by resident fish and invertebrates, provides an important cue for orientation and habitat selection during this process, which must often occur in environments impacted by anthropogenic noise. We adapted an established field-based protocol to test whether recorded boat noise influenced the settlement behavior of reef fish. Fewer fish settled to patch reefs broadcasting boat + reef noise compared with reef noise alone. This study suggests that boat noise, now a common feature of many reefs, can compromise critical settlement behavior of reef fishes.

Damsel in distress: captured damselfish prey emit chemical cues that attract secondary predators and improve escape chances.

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.

Background level of risk and the survival of predator-naive prey: can neophobia compensate for predator naivety in juvenile coral reef fishes?

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.

Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities.

Ocean warming and acidification are serious threats to marine life. While each stressor alone has been studied in detail, their combined effects on the outcome of ecological interactions are poorly understood. We measured predation rates and predator selectivity of two closely related species of damselfish exposed to a predatory dottyback. We found temperature and CO2 interacted synergistically on overall predation rate, but antagonistically on predator selectivity. Notably, elevated CO2 or temperature alone reversed predator selectivity, but the interaction between the two stressors cancelled selectivity. Routine metabolic rates of the two prey showed strong species differences in tolerance to CO2 and not temperature, but these differences did not correlate with recorded mortality. This highlights the difficulty of linking species-level physiological tolerance to resulting ecological outcomes. This study is the first to document both synergistic and antagonistic effects of elevated CO2 and temperature on a crucial ecological process like predator-prey dynamics.

Presence of cleaner wrasse increases the recruitment of damselfishes to coral reefs.

Mutualisms affect the biodiversity, distribution and abundance of biological communities. However, ecological processes that drive mutualism-related shifts in population structure are often unclear and must be examined to elucidate how complex, multi-species mutualistic networks are formed and structured. In this study, we investigated how the presence of key marine mutualistic partners can drive the organisation of local communities on coral reefs. The cleaner wrasse, Labroides dimidiatus, removes ectoparasites and reduces stress hormones for multiple reef fish species, and their presence on coral reefs increases fish abundance and diversity. Such changes in population structure could be driven by increased recruitment of larval fish at settlement, or by post-settlement processes such as modified levels of migration or predation. We conducted a controlled field experiment to examine the effect of cleaners on recruitment processes of a common group of reef fishes, and showed that small patch reefs (61-285 m(2)) with cleaner wrasse had higher abundances of damselfish recruits than reefs from which cleaner wrasse had been removed over a 12-year period. However, the presence of cleaner wrasse did not affect species diversity of damselfish recruits. Our study provides evidence of the ecological processes that underpin changes in local population structure in the presence of a key mutualistic partner.