Search

A prerequisite for effective antipredator responses is the ability of a prey to distinguish animals that pose a threat from those that do not. Prey often have efficient learning mechanisms to learn threats but learning to recognize nonpredators may be equally or more important. Moreover, the ability to generalize learned information is of key importance for prey animals. Prey take information they know about one species to make ‘educated guesses’ about the predatory/nonpredatory status of other unknown species. Here, we investigate the ability of Whitetail damselfish Pomacentrus chrysurus to learn the identity of non‐predators and then generalize their responses to other unknown animals. Our work is completed within the context of unprecedented habitat degradation in reef ecosystems. When corals die, the remaining skeleton is colonized by algae, cyanobacteria and sessile invertebrates. These opportunistic colonists change the physical and chemical landscape of the reef and hence the background odour in which predator and non‐predator recognition occurs. Our results indicated that Whitetail damselfish learn to classify Moonwrasse Thalasomma lunare as a non‐predator through the process of latent inhibition, whereby the prey are repeatedly exposed to Moonwrasse odour multiple times in the absence of negative reinforcement. These fish subsequently generalized their nonpredator recognition to other unknown wrasse, but not distantly related fish. Of key importance was our finding that the patterns and extent of non‐predator learning and generalization were dramatically altered in dead coral habitats. As predicted, prey that learned the Moonwrasse as a nonpredator in live coral environments did not subsequently respond to Moonwrasse when we tried to teach them Moonwrasse was a predator in live coral. However, this non‐predator recognition was reduced in dead coral environments. Moreover, generalization completely failed when we changed from live to dead coral environments. Juvenile damselfishes need to rapidly catalogue the identity of unknown animals when they arrive at a reef. Changing background odours, that occur with changing tides and currents, means that prey need to learn non‐predator identities separately in each water source. This cognitive challenge likely has significant survival consequence in a changing environment. A free Plain Language Summary can be found within the Supporting Information of this article.

1. An increasing number of coral reefs throughout the world have become degraded as a result of climate change. This degradation has resulted in a significant decline in local biodiversity. Studies have shown that some fishes (non‐responders) within these altered habitats are not able to adequately access olfactory cues, specifically chemical alarm cues that are crucial in mediating predation risk. 2. We propose that the inability to access this crucial information is a potential mechanism for increased mortality of these species under natural conditions. However, we posit that the presence of certain key species (responders that are unaffected by degradation) may buffer the handicap of non‐responders by providing an alternate source of information. 3. To explore this hypothesis, we investigated if a high ratio of responders to non‐responders could mitigate the impact of information loss for the affected species. Using mesocosms, we manipulated the ratio of two damselfish species, Pomacentrus chrysurus (responder) and P. moluccensis (non‐responder), to determine if community composition can be predictive of information transfer about predation threats in nearby non‐responder individuals. 4. Our results indicate that, in degraded environments, the magnitude of fear effects seen in P. moluccensis exposed to a predator was proportional to the number of P. chrysurus present and consumed by the predator in the community. This indicates that P. chrysurus became the only functional source of predation‐related information for P. moluccensis in degraded habitats. These results contrasted with those from live coral environments, where all individuals exhibited fear effects, regardless of community composition. 5. Our study provides evidence that the presence of non‐affected species in the community provides a potential mechanism allowing increased resilience by affected species, therefore providing another example of the way biodiversity affects ecological resilience of species in changing ecosystems.

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 change in coral reefs from live coral to algal-dominated seascapes prevents some fish species from using chemical alarm cues to gain information about their risk of predation. Field experiments showed that Ambon damselfish, Pomacentrus amboinensis, were able to learn the identity of individual novel predators from a cocktail of odours from three predators derived from digestive products. Learning only occurred when the predators had been fed conspecifics of the prey species in the presence of water that had passed over live hard coral. This allows novel predators to be identified long after the immediate capture and ingestion event. Fish that had the same learning opportunity in degraded water took more risk and died faster on habitat patches in the field. Ambon damselfish respond to chemical alarm cues from closely related Pomacentrus nagasakiensis, in both live and degraded water, yet experiments suggested they cannot use the congeneric diet odours to label predators. However, we did find a modest survival benefit under natural conditions, suggesting some limited learning occurred. Findings suggest that as coral habitats degrade, fishes that are affected by the changing chemistry will have a greatly reduced range of mechanisms for obtaining and updating threat information, altering the resilience of communities.

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.

Mortality through predation is often selective, particularly at life-history bottlenecks. While many studies have looked at the importance for survival of specific prey characteristics in isolation, few have looked at a broad array of attributes and how they relate to survival in a realistic context. Our study measures 18 morphological, performance and behavioural traits of a juvenile damselfish that have been hypothesized as important for prey survival, and examines how they relate to survival in the field immediately after settlement. These attributes included size, relative false eye-spot size, fast-start escape response kinematics, thigmotaxis, laterality, and space use and activity in the field. Using conditional inference trees, we identify the most important drivers out of a reduced suite of 13 characters. Fast-start response latency, boldness, feeding rates and two measures of activity were found to significantly contribute to survival. Morphological variables and most laboratory measures of performance appeared to contribute little to survival. Results suggest selection works on a suite of characters associated with boldness. Bold and active fish are those that will be best able to learn using public information, but because of the relative naivete of newly metamorphosed fishes, speed to react to a strike from an unknown predator is of critical importance. Findings substantiate the ecomorphological paradigm by suggesting that selection on behaviour modifies the correlations of morphological and performance variables with survival probabilities, since behaviour modifies performance capabilities by making them specific to context.

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 rarely cause direct mortality. Rather, micropredators impose an energetic tax, thus significantly affecting host physiology and behaviour via such 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 would lead 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.

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.

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.

Boat noise is becoming increasingly common and is now recognized as an environmental pollutant (Slabbekoorn et al., 2010). We show, for the first time that boat noise elicits a stress response in fish embryos, and that their stress response is greater upon exposure to 2-stroke engines than 4-stroke engines., Human generated noise is changing the natural underwater soundscapes worldwide. The most pervasive sources of underwater anthropogenic noise are motorboats, which have been found to negatively affect several aspects of fish biology. However, few studies have examined the effects of noise on early life stages, especially the embryonic stage, despite embryo health being critical to larval survival and recruitment. Here, we used a novel setup to monitor heart rates of embryos from the staghorn damselfish (Amblyglyphidodon curacao) in shallow reef conditions, allowing us to examine the effects of in situ boat noise in context with real-world exposure. We found that the heart rate of embryos increased in the presence of boat noise, which can be associated with the stress response. Additionally, we found 2-stroke outboard-powered boats had more than twice the effect on embryo heart rates than did 4-stroke powered boats, showing an increase in mean individual heart rate of 1.9% and 4.6%, respectively. To our knowledge this is the first evidence suggesting boat noise elicits a stress response in fish embryo and highlights the need to explore the ecological ramifications of boat noise stress during the embryo stage. Also, knowing the response of marine organisms caused by the sound emissions of particular engine types provides an important tool for reef managers to mitigate noise pollution.

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.