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

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

Effects of elevated CO2 on predator avoidance behaviour by reef fishes is not altered by experimental test water

Pioneering studies into the effects of elevated CO2 on the behaviour of reef fishes often tested high-CO2 reared fish using control water in the test arena. While subsequent studies using rearing treatment water (control or high CO2) in the test arena have confirmed the effects of high CO2 on a range of reef fish behaviours, a further investigation into the use of different test water in the experimental arena is warranted. Here, we used a fully factorial design to test the effect of rearing treatment water (control or high CO2) and experimental test water (control or high CO2) on antipredator responses of larval reef fishes. We tested antipredator behaviour in larval clownfish Amphiprion percula and ambon damselfish Pomacentrus amboinensis, two species that have been used in previous high CO2 experiments. Specifically, we tested if: (1) using control or high CO2 water in a two channel flume influenced the response of larval clownfish to predator odour; and (2) using control or high CO2 water in the test arena influenced the escape response of larval damselfish to a startle stimulus. Finally, (3) because the effects of high CO2 on fish behaviour appear to be caused by altered function of the GABA-A neurotransmitter we tested if antipredator behaviours were restored in clownfish treated with a GABA antagonist (gabazine) in high CO2 water. Larval clownfish reared from hatching in control water (496 µatm) strongly avoided predator cue whereas larval clownfish reared from hatching in high CO2 (1,022 µatm) were attracted to the predator cue, as has been reported in previous studies. There was no effect on fish responses of using either control or high CO2 water in the flume. Larval damselfish reared for four days in high CO2 (1,051 µatm) exhibited a slower response to a startle stimulus and slower escape speed compared with fish reared in control conditions (464 µatm). There was no effect of test water on escape responses. Treatment of high-CO2 reared clownfish with 4 mg l−1 gabazine in high CO2 seawater restored the normal response to predator odour, as has been previously reported with fish tested in control water. Our results show that using control water in the experimental trials did not influence the results of previous studies on antipredator behaviour of reef fishes and also supports the results of novel experiments conducted in natural reef habitat at ambient CO2 levels

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

The effects of climate change on the ecology of fishes

Ocean warming and acidification are set to reshuffle life on Earth and alter ecological processes that underpin the biodiversity, health, productivity, and resilience of ecosystems. Fishes contribute significantly to marine, estuarine, and freshwater species diversity and the functioning of marine ecosystems, and are not immune to climate change impacts. Whilst considerable effort has been placed on studying the effects of climate change on fishes, much emphasis has been placed on their (eco)physiology and at the organismal level. Fishes are affected by climate change through impacts at various levels of biological organisation and through a large variety of traits, making it difficult to make generalisations regarding fish responses to climate change. Here, we briefly review the current state of knowledge of climate change effects on fishes across a wide range of subfields of fish ecology and evaluate these effects at various scales of biological organisation (from genes to ecosystems). We argue that a more holistic synthesis of the various interconnected subfields of fish ecology and integration of responses at different levels of biological organisation are needed for a better understanding of how fishes and their populations and communities might respond or adapt to the multi-stressor effects of climate change. We postulate that studies using natural analogues of climate change, meta-analyses, advanced integrative modelling approaches, and lessons learned from past extreme climate events could help reveal some general patterns of climate change impacts on fishes that are valuable for management and conservation approaches. Whilst these might not reveal many of the underlying mechanisms responsible for observed biodiversity and community change, their insights are useful to help create better climate adaptation strategies for their preservation in a rapidly changing ocean

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