Effects of maternal stress and cortisol exposure at the egg stage on learning, boldness and neophobia in brook trout

in Behaviour
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The environment experienced by females can have long-lasting effects on offspring phenotype. The objective of this study was to determine if maternal stress-induced behaviour reprogramming in offspring is found in brook char and to test whether cortisol is the main mediator, by separating the potential effects of cortisol from that of other potential maternal factors. We exposed female brook trout (Salvelinus fontinalis) to different parallel treatments during the oogenesis period: undisturbed as controls (1) fed cortisol through food (2) or physically stressed by handling once a week (3). Additionally, we exposed half of the control eggs to a cortisol suspension before fertilisation (4). Cortisol consumption and handling did not elevate either maternal plasma or egg cortisol, although egg cortisol level was significantly increased when eggs were bathed in the suspension. We measured spatial learning and memory, boldness and neophobia in 6 month-old offspring and found no effects of treatments on learning, memory or behaviour. Our results suggest that the relationship between maternal stress, circulating and egg cortisol levels, other maternal factors, and behavioural reprogramming is context and species-specific.

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Figures

  • Experimental design. (A) Representation of the control and treatment groups Salvelinus fontinalis females were divided into. Images are female heads with a clutch of eggs underneath and commercial food pellets to the right. Black filling plus white outlines indicate stress induction or cortisol addition. Treatment number and abbreviations for figures are displayed below images. (B) Representation of how the three female families were divided amongst treatments. (C) Representation of egg and juvenile batches.

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  • Cross-sectional view of the maze system. The maze comprised three walls, each with two doors. One door led to a dead end and the other one allowed passage to the next section. Doors that allowed progression into the maze were outlined with blue tape and a plastic plant represented here as open stars. Fish were introduced into the maze in a glass container represented as the open circle.

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  • (A) Plasma cortisol levels (ng/ml) of Salvelinus fontinalis females at stripping and (B) unfertilised egg cortisol levels (ng/ml). There is no maternal circulating cortisol levels data for treatment 3 because half of the eggs from control females were exposed to cortisol prior to fertilisation. Different letters indicate significant differences between treatments (p<0.01). Data presented as means ± SEM.

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  • Boldness measured as latency (s) for Salvelinus fontinalis juveniles to exit the introductory glass container in the maze system on the first day of training. There are no significant differences between treatments (p0.01). Data presented as means ± SEM (N=16, 19, 13 and 18).

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  • Spatial learning measured as time (s) for Salvelinus fontinalis juveniles to complete the maze system over a 5-day training period. Arms indicate significant differences between days (p<0.01). Data presented as means ± SEM (N=16, 19, 13 and 18).

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  • Spatial memory measured as time (s) for Salvelinus fontinalis juveniles to complete the maze system between the fifth (and last day of training) and the trial after the 2-day break. There are no significant differences between days (p0.01). Data presented as means ± SEM (N=13, 13, 7 and 18).

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  • Spatial learning ability calculated as the difference between the time (s) needed to complete the maze by Salvelinus fontinalis juveniles on the second and the fourth day of training in relation with boldness, measured as latency to exit the glass container on the first day of training. There is no significant effect of boldness on learning ability (p=0.2). Each point is an individual (N=16, 19, 13 and 18).

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