Embryonic exposure to a conspecific alarm cue triggers behavioural plasticity in juvenile rainbow trout

In fish, the presence of predator cues in the parental or juvenile environment engenders plasticity in the expression of fear-related behaviours. Whether these cues may engender developmental plasticity when they are present in the environment of embryos remains unexplored. Here, we tested in rainbow trout, Oncorhynchus mykiss: (1) whether exposure to alarm cues during embryonic stages engendered developmental plasticity; and (2) whether an abiotic stressor could also orient the behavioural development of fry. We divided fertilized eggs into three groups: a control nonstressed group (Control), a group of embryos exposed to a conspecific alarm pheromone (e.g. predator-related cue stressor, PS), and a group of embryos that were chronically air exposed for 1 min (e.g. abiotic stressor, AS). Stressors were applied once a day, 3 times per week from 19 days postfertilization (dpf) until 52 dpf. Between 57 and 143 dpf, and for each individual, we assessed the propensity to express fear responses in different contexts and learning performances. When exposed to a novel environment or a novel object, PS fish showed significantly less fear-related behaviour, less freezing and higher activity levels than Control fish. PS fish also showed slower acquisition of a learning task than controls. AS fish did not differ from controls in any test situation. Our results show that in ovo exposure to a natural but not an abiotic signal is a prominent inducer of rainbow trout behavioural plasticity across a number of contexts. Our study provides evidence that the expression of neophobia by fish fry may be modulated by the level of risk perceived by embryos in the environment.