Impact of ocean warming on a coral reef fish learning and memory.

Tropical ectotherms are highly sensitive to environmental warming, especially coral reef fishes, which are negatively impacted by an increase of a few degrees in ocean temperature. However, much of our understanding on the thermal sensitivity of reef fish is focused on a few traits (e.g., metabolism, reproduction) and we currently lack knowledge on warming effects on cognition, which may endanger decision-making and survival. Here, we investigated the effects of warming on learning and memory in a damselfish species, Acanthochromis polyacanthus. Fish were held at 28-28.5 °C (control group), 30-30.5 °C (moderate warming group) or 31.5-32 °C (high warming group) for 2 weeks, and then trained to associate a blue tag (cue) to the presence of a conspecific (reward). Following 20 training trials (5 days), fish were tested for associative learning (on the following day) and memory storage (after a 5-days interval). The control group A. polyacanthus showed learning of the task and memory retention after five days, but increasing water temperature impaired learning and memory. A thorough understanding of the effects of heat stress, cognition, and fitness is urgently required because cognition may be a key factor determining animals' performance in the predicted scenario of climate changes. Knowing how different species respond to warming can lead to better predictions of future community dynamics, and because it is species specific, it could pinpoint vulnerable/resilience species.

Habitat complexity and predator odours impact on the stress response and antipredation behaviour in coral reef fish.

Mass coral bleaching events coupled with local stressors have caused regional-scale loss of corals on reefs globally. Following the loss of corals, the structural complexity of these habitats is often reduced. By providing shelter, obscuring visual information, or physically impeding predators, habitat complexity can influence predation risk and the perception of risk by prey. Yet little is known on how habitat complexity and risk assessment interact to influence predator-prey interactions. To better understand how prey's perception of threats may shift in degraded ecosystems, we reared juvenile Pomacentrus chrysurus in environments of various habitat complexity levels and then exposed them to olfactory risk odours before simulating a predator strike. We found that the fast-start escape responses were enhanced when forewarned with olfactory cues of a predator and in environments of increasing complexity. However, no interaction between complexity and olfactory cues was observed in escape responses. To ascertain if the mechanisms used to modify these escape responses were facilitated through hormonal pathways, we conducted whole-body cortisol analysis. Cortisol concentrations interacted with habitat complexity and risk odours, such that P. chrysurus exhibited elevated cortisol levels when forewarned with predator odours, but only when complexity levels were low. Our study suggests that as complexity is lost, prey may more appropriately assess predation risk, likely as a result of receiving additional visual information. Prey's ability to modify their responses depending on the environmental context suggests that they may be able to partly alleviate the risk of increased predator-prey interactions as structural complexity is reduced.

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.

Contrasting hydrodynamic regimes of submerged pinnacle and emergent coral reefs.

Hydrodynamics on coral reefs vary with depth, reef morphology and seascape position. Differences in hydrodynamic regimes strongly influence the structure and function of coral reef ecosystems. Submerged coral reefs on steep-sided, conical bathymetric features like seamounts experience enhanced water circulation as a result of interactions between currents and the abrupt physical structure. There may also be similar interactions between smaller pinnacles and regional water currents in offshore locations (crests > 10 m), while shallow reefs (crests <10 m) may be more subject to surface currents driven by wind, waves and tide. Here we tested whether coral pinnacles experienced stronger and more variable currents compared to emergent reefs at the same depth in both nearshore and offshore positions. Current speeds and temperature were monitored for 12 months at 11 reefs, representing the three different reef categories: submerged offshore pinnacles, emergent offshore reefs and emergent nearshore reefs. We found different patterns in current speeds and temperature among reef types throughout the year and between seasons. Submerged pinnacles exhibited stronger, more variable current speeds compared to both near and offshore emergent reefs. We found seasonal changes in current speeds for pinnacle and nearshore reefs but no variation in current strength on offshore reefs. Whilst instantaneous current directions did reflect the seascape position of individual sites, there was no difference in the directional variability of current speeds between reef types. Annual daily average temperatures at all reef types were not strongly seasonal, changing by less than 2 °C throughout the year. Daily temperature ranges at specific sites however, exhibited considerable variability (annual range of up to 6.5 °C), particularly amongst offshore emergent reefs which experienced the highest temperatures despite greater exposure to regional-scale circulation patterns. Additionally, we found a consistent mismatch between satellite sea surface temperatures and in-situ temperature data, which was on average 2 °C cooler throughout the annual study period. Our results suggest that distinct hydrodynamic processes occur on smaller submerged structures that are physically analogous to seamounts. Our findings highlight important nuances in environmental processes that occur on morphologically distinct coral reef habitats and these are likely to be important drivers for the community dynamics of organisms that inhabit these reefs.

Limiting motorboat noise on coral reefs boosts fish reproductive success.

Anthropogenic noise impacts are pervasive across taxa, ecosystems and the world. Here, we experimentally test the hypothesis that protecting vulnerable habitats from noise pollution can improve animal reproductive success. Using a season-long field manipulation with an established model system on the Great Barrier Reef, we demonstrate that limiting motorboat activity on reefs leads to the survival of more fish offspring compared to reefs experiencing busy motorboat traffic. A complementary laboratory experiment isolated the importance of noise and, in combination with the field study, showed that the enhanced reproductive success on protected reefs is likely due to improvements in parental care and offspring length. Our results suggest noise mitigation could have benefits that carry through to the population-level by increasing adult reproductive output and offspring growth, thus helping to protect coral reefs from human impacts and presenting a valuable opportunity for enhancing ecosystem resilience.

Living in mixed species groups promotes predator learning in degraded habitats.

Living in mix-species aggregations provides animals with substantive anti-predator, foraging and locomotory advantages while simultaneously exposing them to costs, including increased competition and pathogen exposure. Given each species possess unique morphology, competitive ability, parasite vulnerability and predator defences, we can surmise that each species in mixed groups will experience a unique set of trade-offs. In addition to this unique balance, each species must also contend with anthropogenic changes, a relatively new, and rapidly increasing phenomenon, that adds further complexity to any system. This complex balance of biotic and abiotic factors is on full display in the exceptionally diverse, yet anthropogenically degraded, Great Barrier Reef of Australia. One such example within this intricate ecosystem is the inability of some damselfish to utilize their own chemical alarm cues within degraded habitats, leaving them exposed to increased predation risk. These cues, which are released when the skin is damaged, warn nearby individuals of increased predation risk and act as a crucial associative learning tool. Normally, a single exposure of alarm cues paired with an unknown predator odour facilitates learning of that new odour as dangerous. Here, we show that Ambon damselfish, Pomacentrus amboinensis, a species with impaired alarm responses in degraded habitats, failed to learn a novel predator odour as risky when associated with chemical alarm cues. However, in the same degraded habitats, the same species learned to recognize a novel predator as risky when the predator odour was paired with alarm cues of the closely related, and co-occurring, whitetail damselfish, Pomacentrus chrysurus. The importance of this learning opportunity was underscored in a survival experiment which demonstrated that fish in degraded habitats trained with heterospecific alarm cues, had higher survival than those we tried to train with conspecific alarm cues. From these data, we conclude that redundancy in learning mechanisms among prey guild members may lead to increased stability in rapidly changing environments.

Social familiarity improves fast-start escape performance in schooling fish.

Using social groups (i.e. schools) of the tropical damselfish Chromis viridis, we test how familiarity through repeated social interactions influences fast-start responses, the primary defensive behaviour in a range of taxa, including fish, sharks, and larval amphibians. We focus on reactivity through response latency and kinematic performance (i.e. agility and propulsion) following a simulated predator attack, while distinguishing between first and subsequent responders (direct response to stimulation versus response triggered by integrated direct and social stimulation, respectively). In familiar schools, first and subsequent responders exhibit shorter latency than unfamiliar individuals, demonstrating that familiarity increases reactivity to direct and, potentially, social stimulation. Further, familiarity modulates kinematic performance in subsequent responders, demonstrated by increased agility and propulsion. These findings demonstrate that the benefits of social recognition and memory may enhance individual fitness through greater survival of predator attacks.

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.

Assessing and mitigating impacts of motorboat noise on nesting damselfish.

Motorboats are a pervasive, growing source of anthropogenic noise in marine environments, with known impacts on fish physiology and behaviour. However, empirical evidence for the disruption of parental care remains scarce and stems predominantly from playback studies. Additionally, there is a paucity of experimental studies examining noise-mitigation strategies. We conducted two field experiments to investigate the effects of noise from real motorboats on the parental-care behaviours of a common coral-reef fish, the Ambon damselfish Pomacentrus amboinensis, which exhibits male-only egg care. When exposed to motorboat noise, we found that males exhibited vigilance behaviour 34% more often and spent 17% more time remaining vigilant, compared to an ambient-sound control. We then investigated nest defence in the presence of an introduced conspecific male intruder, incorporating a third noise treatment of altered motorboat-driving practice that was designed to mitigate noise exposure via speed and distance limitations. The males spent 22% less time interacting with the intruder and 154% more time sheltering during normal motorboat exposure compared to the ambient-sound control, with nest-defence levels in the mitigation treatment equivalent to those in ambient conditions. Our results reveal detrimental impacts of real motorboat noise on some aspects of parental care in fish, and successfully demonstrate the positive effects of an affordable, easily implemented mitigation strategy. We strongly advocate the integration of mitigation strategies into future experiments in this field, and the application of evidence-based policy in our increasingly noisy world.

Vessel noise affects routine swimming and escape response of a coral reef fish.

An increasing number of studies have shown that anthropogenic noise can negatively affect aspects of the anti-predator behaviour of reef fishes, potentially affecting fitness and survival. However, it has been suggested that effects could differ among noise sources. The present study compared two common sources of anthropogenic noise and investigated its effects on behavioural traits critical for fish survival. In a tank-based experiment we examined the effects of noise from 4-stroke motorboats and ships (bulk carriers > 50,000 tonnes) on the routine swimming and escape response of a coral reef fish, the whitetail damselfish (Pomacentrus chrysurus). Both 4-stroke boat and ship noise playbacks affected the fast-start response and routine swimming of whitetail damselfish, however the magnitude of the effects differed. Fish exposed to ship noise moved shorter distances and responded more slowly (higher response latency) to the startle stimulus compared to individuals under the 4-stroke noise treatment. Our study suggests that 4-stroke and ship noise can affect activity and escape response of individuals to a simulated predation threat, potentially compromising their anti-predator behaviour.

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.

Parents know best: transgenerational predator recognition through parental effects.

In highly biodiverse systems, such as coral reefs, prey species are faced with predatory threats from numerous species. Recognition of predators can be innate, or learned, and can help increase the chance of survival. Research suggests that parental exposure to increased predatory threats can affect the development, behaviour, and ultimately, success of their offspring. Breeding pairs of damselfish (Acanthochromis polyacanthus) were subjected to one of three olfactory and visual treatments (predator, herbivore, or control), and their developing embryos were subsequently exposed to five different chemosensory cues. Offspring of parents assigned to the predator treatment exhibited a mean increase in heart rate two times greater than that of offspring from parents in herbivore or control treatments. This increased reaction to a parentally known predator odour suggests that predator-treated parents passed down relevant threat information to their offspring, via parental effects. This is the first time transgenerational recognition of a specific predator has been confirmed in any species. This phenomenon could influence predator-induced mortality rates and enable populations to adaptively respond to fluctuations in predator composition and environmental changes.

Acoustic enrichment can enhance fish community development on degraded coral reef habitat.

Coral reefs worldwide are increasingly damaged by anthropogenic stressors, necessitating novel approaches for their management. Maintaining healthy fish communities counteracts reef degradation, but degraded reefs smell and sound less attractive to settlement-stage fishes than their healthy states. Here, using a six-week field experiment, we demonstrate that playback of healthy reef sound can increase fish settlement and retention to degraded habitat. We compare fish community development on acoustically enriched coral-rubble patch reefs with acoustically unmanipulated controls. Acoustic enrichment enhances fish community development across all major trophic guilds, with a doubling in overall abundance and 50% greater species richness. If combined with active habitat restoration and effective conservation measures, rebuilding fish communities in this manner might accelerate ecosystem recovery at multiple spatial and temporal scales. Acoustic enrichment shows promise as a novel tool for the active management of degraded coral reefs.

Habitat degradation and predators have independent trait-mediated effects on prey.

Coral reefs are degrading globally leading to a catastrophic loss of biodiversity. While shifts in the species composition of communities have been well documented associated with habitat change, the mechanisms that underlie change are often poorly understood. Our study experimentally examines the effects of coral degradation on the trait-mediated effects of predators on the morphology, behaviour and performance of a juvenile coral reef fish. Juvenile damselfish were exposed to predators or controls (omnivore or nothing) in seawater that had flowed over either live or dead-degraded coral over a 45d period. No interaction between water source and predator exposure was found. However, fish exposed to degraded water had larger false eyespots relative to the size of their true eyes, and were more active, both of which may lead to a survival advantage. Non-consumptive effects of predators on prey occurred regardless of water source and included longer and deeper bodies, large false eyespots that may distract predator strikes away from the vulnerable head region, and shorter latencies in their response to a simulated predator strike. Research underscores that phenotypic plasticity may assist fishes in coping with habitat degradation and promote greater resilience to habitat change than may otherwise be predicted.

The effect of climate change on the escape kinematics and performance of fishes: implications for future predator-prey interactions.

Climate change can have a pronounced impact on the physiology and behaviour of fishes. Notably, many climate change stressors, such as global warming, hypoxia and ocean acidification (OA), have been shown to alter the kinematics of predator-prey interactions in fishes, with potential effects at ecological levels. Here, we review the main effects of each of these stressors on fish escape responses using an integrative approach that encompasses behavioural and kinematic variables. Elevated temperature was shown to affect many components of the escape response, including escape latencies, kinematics and maximum swimming performance, while the main effect of hypoxia was on escape responsiveness and directionality. OA had a negative effect on the escape response of juvenile fish by decreasing their directionality, responsiveness and locomotor performance, although some studies show no effect of acidification. The few studies that have explored the effects of multiple stressors show that temperature tends to have a stronger effect on escape performance than OA. Overall, the effects of climate change on escape responses may occur through decreased muscle performance and/or an interference with brain and sensory functions. In all of these cases, since the escape response is a behaviour directly related to survival, these effects are likely to be fundamental drivers of changes in marine communities. The overall future impact of these stressors is discussed by including their potential effects on predator attack behaviour, thereby allowing the development of potential future scenarios for predator-prey interactions.

Intrageneric differences in the effects of acute temperature exposure on competitive behaviour of damselfishes.

Projected increases in global temperatures brought on by climate change threaten to disrupt many biological and ecological processes. Tropical ectotherms, like many fishes, can be particularly susceptible to temperature change as they occupy environments with narrow thermal fluctuations. While climate change models predict temperatures to increase over decades, thermal fluctuations are already experienced on a seasonal scale, which may affect the ability to capture and defend resources across a thermal gradient. For coral reef fish, losers of competitive interactions are often more vulnerable to predation, and this pressure is strongest just after settlement. Competitive interactions may determine future success for coral reef fishes, and understanding how temperature experienced during settlement can influence such interactions will give insight to community dynamics in a future warmer world. We tested the effect of increased temperatures on intraspecific competitive interactions of two sympatric species of reef damselfish, the blue damselfish Pomacentrus nagasakiensis, and the whitetail damselfish Pomacentrus chrysurus. Juvenile fishes were exposed to one of four temperature treatments, ranging from 26-32 °C, for seven days then placed into competitive arenas where aggressive interactions were recorded between sized matched individuals within each species. While there was no apparent effect of temperature treatment on aggressive behaviour for P. chrysurus, we observed up to a four-fold increase in aggression scores for P. nagasakiensis with increasing temperature. Results suggest that temperature experienced as juveniles can impact aggressive behaviour; however, species-specific thermal tolerances led to behavioural affects that differ among closely related species. Differential thermal tolerance among species may cause restructuring of the interaction network that underlies the structure of reef assemblages.

Effects of boat noise on fish fast-start escape response depend on engine type.

Vessel noise represents a relatively recent but rapidly increasing form of pollution, which affects the many organisms that use sound to inform their behavioural decisions. Recent research shows that anthropogenic noise can lead to reduced responsiveness to risk and higher mortality. The current laboratory experiment determined whether the playback of noise from motorboats powered by two- or four-stroke outboard engines affected the kinematics of the fast-start response in a juvenile coral reef fish, and the time scale over which the effects may occur. Results show that the two engine types produce slightly different sound spectra, which influence fish differently. Playback of 2-stroke engines had the greatest effect on activity, but only for a brief period (45 s). While noise from 4-stroke outboard engines affected fast-start kinematics, they had half the impact of noise from 2-stroke engines. Two-stroke engine noise affected routine swimming more than 4-stroke engines, while 4-stroke noise had a greater effect on the speed at which fish responded to a startle. Evidence suggests that the source of the noise pollution will have a major influence on the way marine organisms will respond, and this gives managers an important tool whereby they may reduce the effects of noise pollution on protected communities.

A negative correlation between behavioural and physiological performance under ocean acidification and warming.

Many studies have examined the average effects of ocean acidification and warming on phenotypic traits of reef fishes, finding variable, but often negative effects on behavioural and physiological performance. Yet the presence and nature of a relationship between these traits is unknown. A negative relationship between phenotypic traits could limit individual performance and even the capacity of populations to adapt to climate change. Here, we examined the relationship between behavioural and physiological performance of a juvenile reef fish under elevated CO2 and temperature in a full factorial design. Behaviourally, the response to an alarm odour was negatively affected by elevated CO2, but not elevated temperature. Physiologically, aerobic scope was significantly diminished under elevated temperature, but not under elevated CO2. At the individual level, there was no relationship between behavioural and physiological traits in the control and single-stressor treatments. However, a statistically significant negative relationship was detected between the traits in the combined elevated CO2 and temperature treatment. Our results demonstrate that trade-offs in performance between behavioural and physiological traits may only be evident when multiple climate change stressors are considered, and suggest that this negative relationship could limit adaptive potential to climate change.

Relative influence of environmental factors on the timing and occurrence of multi-species coral reef fish aggregations.

Reef configuration and hydrodynamics were identified as the principle physical drivers behind coral reef fish aggregations on a mid-shelf patch reef in the northern section of the Great Barrier Reef (-16.845°, 146.23°). The study was carried out over a six-year period at a large reef pass on the oceanic margin of the northern Great Barrier Reef. Over this period (February 2006 -December 2012) tidal state, moon phase and surface seawater temperature were monitored. The timing of sampling was organised to assess variation in physical environment at daily, monthly, seasonal and annual time scales. Over these time scales, temporal patterns of occurrence of 10 species of coral reef fish from 5 families representing 5 defined trophic groups were monitored. The study incorporated 1,357 underwater visual census counts involving 402,370 fish and these estimates were collated with data on tidal state, water temperature, lunar and seasonal periodicity. Aggregated boosted regression trees analysed the univariate responses of fish abundance and species richness to the variation in the physical environment of the reef pass. Flood tides or when water flows from open water through the pass and into the Moore Reef lagoon had 2.3 times as many fish and 1.75 times as many species compared to counts made on ebb tides. Fish abundance was highest in late winter and spring months (Austral calendar), but notably when water temperatures were below the long-term mean of 27°C. Multivariate regression trees and Dufrêne-Legendre indicator predicted 4 out of 10 times the occurrence of all 10 species at any temporal scale ranging from hours to years. Flood tides were the principle driver underlying the occurrence of all 10 species regardless of their trophic classification and produced distinct seasonal assemblages, indicative of fishes aggregating to forage and reproduce.