Interspecific differences in how habitat degradation affects escape response

Degradation of habitats is widespread and a leading cause of extinctions. Our study determined whether the change in the chemical landscape associated with coral degradation affected the way three fish species use olfactory information to optimize their fast-start escape response. Water from degraded coral habitats affected the fast-start response of the three closely-related damselfishes, but its effect differed markedly among species. The Ward's damselfish (Pomacentrus wardi) was most affected by water from degraded coral, and displayed shorter distances covered in the fast-start and slower escape speeds compared to fish in water from healthy coral. In the presence of alarm odours, which indicate an imminent threat, the Ambon damsel (P. amboinensis) displayed enhanced fast-start performance in water from healthy coral, but not when in water from degraded coral. In contrast, while the white-tailed damsel (P. chrysurus) was similarly primed by its alarm odour, the elevation of fast start performance was not altered by water from degraded coral. These species-specific responses to the chemistry of degraded water and alarm odours suggest differences in the way alarm odours interact with the chemical landscape, and differences in the way species balance information about threats, with likely impacts on the survival of affected species in degraded habitats

Feeling the heat: the effect of acute temperature changes on predator–prey interactions in coral reef fish

Recent studies demonstrate that the elevated temperatures predicted to occur by the end of the century can affect the physiological performance and behaviour of larval and juvenile fishes; however, little is known of the effect of these temperatures on ecological processes, such as predator–prey interactions. Here, we show that exposure to elevated temperatures significantly affected the predator–prey interactions of a pair of common reef fish, the planktivorous damselfish (Pomacentrus wardi) and the piscivorous dottyback (Pseudochromis fuscus). When predators exposed to elevated temperatures interacted with prey exposed in a similar manner, maximal attack speeds increased. This effect coupled with decreasing prey escape speeds and escape distances led to increased predation rates. Prey exposed to elevated temperatures also had decreased reaction distances and increased apparent looming threshold, suggesting that their sensory performance was affected. This occurred despite the increase in maximal attack speeds, which in other species has been shown to increase reaction distances. These results suggest that the escape performance of prey is sensitive to short-term increases in ambient temperature. As marine environments become more thermally variable in the future, our results demonstrate that some predators may become more successful, suggesting that there will be strong selection for the maintenance of maximal escape performance in prey. In the present era of rapid climate change, understanding how changes to individual performance influence the relationships between predators and their prey will be increasingly important in predicting the effects of climate change within ecosystems

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

Risk assessment and predator learning in a changing world: understanding the impacts of coral reef degradation

Habitat degradation is among the top drivers of the loss of global biodiversity. This problem is particularly acute in coral reef system. Here we investigated whether coral degradation influences predator risk assessment and learning for damselfish. When in a live coral environment, Ambon damselfish were able to learn the identity of an unknown predator upon exposure to damselfish alarm cues combined with predator odour and were able to socially transmit this learned recognition to naïve conspecifics. However, in the presence of dead coral water, damselfish failed to learn to recognize the predator through alarm cue conditioning and hence could not transmit the information socially. Unlike alarm cues of Ambon damselfish that appear to be rendered unusable in degraded coral habitats, alarm cues of Nagasaki damselfish remain viable in this same environment. Nagasaki damselfish were able to learn predators through conditioning with alarm cues in degraded habitats and subsequently transmit the information socially to Ambon damselfish. Predator-prey dynamics may be profoundly affected as habitat degradation proceeds; the success of one species that appears to have compromised predation assessment and learning, may find itself reliant on other species that are seemingly unaffected by the same degree of habitat degradation

Living in a risky world: the onset and ontogeny of an integrated antipredator phenotype in a coral reef fish

Prey individuals with complex life-histories often cannot predict the type of risk environment to which they will be exposed at each of their life stages. Because the level of investment in defences should match local risk conditions, we predict that these individuals should have the ability to modulate the expression of an integrated defensive phenotype, but this switch in expression should occur at key life-history transitions. We manipulated background level of risk in juvenile damselfish for four days following settlement (a key life-history transition) or 10 days post-settlement, and measured a suite of physiological and behavioural variables over 2 weeks. We found that settlement-stage fish exposed to high-risk conditions displayed behavioural and physiological alterations consistent with high-risk phenotypes, which gave them a survival advantage when exposed to predators. These changes were maintained for at least 2 weeks. The same exposure in post-settlement fish failed to elicit a change in some traits, while the expression of other traits disappeared within a week. Our results are consistent with those expected from phenotypic resonance. Expression of antipredator traits may be masked if individuals are not exposed to certain conditions at key ontogenetic stages

Organ health and development in larval kingfish are unaffected by ocean acidification and warming

Anthropogenic CO₂ emissions are causing global ocean warming and ocean acidification. The early life stages of some marine fish are vulnerable to elevated ocean temperatures and CO₂ concentrations, with lowered survival and growth rates most frequently documented. Underlying these effects, damage to different organs has been found as a response to elevated CO₂ in larvae of several species of marine fish, yet the combined effects of acidification and warming on organ health are unknown. Yellowtail kingfish, Seriola lalandi, a circumglobal subtropical pelagic fish of high commercial and recreational value, were reared from fertilization under control (21 °C) and elevated (25 °C) temperature conditions fully crossed with control (500 µatm) and elevated (1,000 µatm) pCO₂ conditions. Larvae were sampled at 11 days and 21 days post hatch for histological analysis of the eye, gills, gut, liver, pancreas, kidney and liver. Previous work found elevated temperature, but not elevated CO₂, significantly reduced larval kingfish survival while increasing growth and developmental rate. The current histological analysis aimed to determine whether there were additional sublethal effects on organ condition and development and whether underlying organ damage could be responsible for the documented effects of temperature on survivorship. While damage to different organs was found in a number of larvae, these effects were not related to temperature and/or CO₂ treatment. We conclude that kingfish larvae are generally vulnerable during organogenesis of the digestive system in their early development, but that this will not be exacerbated by near-future ocean warming and acidification

Indirect predator effects influence behaviour but not morphology of juvenile coral reef Ambon damselfish Pomacentrus amboinensis

A 6-week laboratory experiment exposed juvenile Ambon damselfish Pomacentrus amboinensis to visual and chemical cues of either a predator, a herbivore or a null control (sea water) and found no effect of predator cues on prey morphology (proportion of ocellus to eye diameter, body depth, standard length and fin area). Nonetheless, behaviour was significantly affected by predator presence, with prey less active and taking half as many feeding strikes when exposed to predators compared to fish from the null control. The presence of a herbivore also affected prey behaviour similar to that of the predator, suggesting that the presence of a non-predator may have important effects on development

Plasticity of escape responses: prior predator experience enhances escape performance in a coral reef fish

Teleost and amphibian prey undertake fast-start escape responses during a predatory attack in an attempt to avoid being captured. Although previously viewed as a reflex reaction controlled by the autonomic nervous system, the escape responses of individuals when repeatedly startled are highly variable in their characteristics, suggesting some behavioural mediation of the response. Previous studies have shown that fishes are able to learn from past experiences, but few studies have assessed how past experience with predators affect the fast-start response. Here we determined whether prior experience with the smell or sight of a predator (the Dottyback, Pseudochromis fuscus) affected the escape response of juveniles of the Spiny Chromis (Acanthochromis polyacanthus). Results show that individuals exposed to any of the predator cues prior to being startled exhibited a stronger escape response (i.e., reduced latency, increased escape distance, mean response speed, maximum response speed and maximum acceleration) when compared with controls. This study demonstrates the plasticity of escape responses and highlights the potential for naive reef fish to take into account both visual and olfactory threat cues simultaneously to optimise the amplitude of their kinematic responses to perceived risk

Oil exposure disrupts early life-history stages of coral reef fishes via behavioural impairments

Global demand for energy and oil-based products is progressively introducing petrogenic polycyclic aromatic hydrocarbons (PAHs) into sensitive marine environments, primarily from fossil-fuel exploration, transport, and urban and industrial runoff. These toxic pollutants are found worldwide, yet the long-term ecological effects on coral reef ecosystems are unknown. Here, we demonstrate that oil exposure spanning PAH concentrations that are environmentally relevant for many coastal marine ecosystems (<= 5.7 mu g I-1), including parts of the Great Barrier Reef, Red Sea, Asia and the Caribbean, causes elevated mortality and stunted growth rates in six species of pre-settlement coral reef fishes, spanning two evolutionarily distinct families (Pomacentridae and Lethrinidae). Furthermore, oil exposure alters habitat settlement and antipredator behaviours, causing reduced sheltering, shoaling and increased risk taking, all of which exacerbate predator-induced mortality during recruitment. These results suggest a previously unknown path, whereby oil and PAH exposure impair higher-order cognitive processing and behaviours necessary for the successful settlement and survival of larval fishes. This emphasizes the risks associated with industrial activities within at-risk ecosystems