Background level of risk determines how prey categorize predators and non-predators.

Much of the plasticity that prey exhibit in response to predators is linked to the prey's immediate background level of risk. However, we know almost nothing of how background risk influences how prey learn to categorize predators and non-predators. Learning non-predators probably represents one of the most underappreciated aspects of anti-predator decision-making. Here, we provide larval damselfish (Pomacentrus chrysurus) with a high or low background risk and then try to teach them to recognize a cue as non-threatening through the process of latent inhibition. Prey from the low-risk background that were pre-exposed to the novel odour cues in the absence of negative reinforcement for 3 days, and then provided the opportunity to learn to recognize the odour as threatening, failed to subsequently respond to the odour as a threat. Fish from the high-risk background showed a much different response. These fish did not learn the odour as non-threatening, probably because the cost of falsely learning an odour as non-threatening is higher when the background level of risk is higher. Our work highlights that background level of risk appears to drive plasticity in cognition of prey animals learning to discriminate threats in their environment.

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 naïve reef fish to take into account both visual and olfactory threat cues simultaneously to optimise the amplitude of their kinematic responses to perceived risk.

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.

Temporal constraints on predation risk assessment in a changing world.

Habitat degradation takes various forms and likely represents the most significant threat to our global biodiversity. Recently, we have seen considerable attention paid to increasing global CO2 emissions which lead to ocean acidification (OA). Other stressors, such as changing levels of ultraviolet radiation (UVR), also impact biodiversity but have received much less attention in the recent past. Here we examine fundamental questions about temporal aspects of risk assessment by coral reef damselfish and provide critical insights into how OA and UVR influence this assessment. Chemical cues released during a predator attack provide a rich source of information that other prey animals use to mediate their risk of predation and are the basis of the majority of trait-mediated indirect interactions in aquatic communities. However, we have surprisingly limited information about temporal aspects of risk assessment because we lack knowledge about how long chemical cues persist after they are released into the environment. Here, we showed that under ambient CO2 conditions (~385 µatm), alarm cues of ambon damselfish (Pomacentrus amboinensis) did not degrade within 30 min in the absence of ultraviolet radiation (UVR), but were degraded within 15 min when the CO2 was increased to ~905 µatm. In experiments that used filters to eliminate UVR, we found minimal degradation of alarm cues within 30 min, whereas under ambient UVR conditions, alarm cues were completely degraded within 15 min. Moreover, in the presence of both UVR and elevated CO2, alarm cues were broken down within 5 min. Our results highlight that alarm cues degrade surprisingly quickly under natural conditions and that anthropogenic changes have the potential to dramatically change rates of cue degradation in the wild. This has considerable implications for risk assessment and consequently the importance of trait-mediated indirect interactions in coral-reef communities.