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

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

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

Diet cues and their utility for risk assessment in degraded habitats

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

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

Abstract 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

Coral degradation impairs learning of non-predators by Whitetail damselfish

1: 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. 2: 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. 3: 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. 4: 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

The fading of fear effects due to coral degradation is modulated by community composition

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

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