Coping with change: The influence of early experience, nutrition and stress on behavioral flexibility

When organisms face environmental challenges, they need extra energy to cope. This is provided by the release of stress hormones, like cortisol. These hormones also improve attention and learning, helping the organism to adapt to the new environmental challenge with flexibility in behaviour. Once the challenge is over, cortisol levels return to normal. This quick rise and fall of cortisol is known as stress response. However, if cortisol levels remain high, it can lead to negative effects. Chronic high levels of cortisol can impair learning and overall health. Models predict that early life stressors as well as an individual’s nutritional status influence stress responses and learning, but their relationships have not been studied. To investigate this relationship between stress exposure, early experiences, nutritional state, and behavioural flexibility, we conducted experiments using a social fish called the “Princess of Lake Tanganyika”. These fish live in groups with parents, their young, and helper fish that assist in raising the young. We chose this species because (i) physiological mechanisms to cope with stress are similar in fish and other vertebrates including humans and (ii) they display a huge diversity of sociocognitive abilities. To investigate the effect of early experience on stress responses later in life, we manipulated early life stress of individual fish in terms of the presence or absence of older group members during the first two months of their lives. When these fish were adults, we exposed them to a stressor and examined their stress responses. We found that experiencing early-life stress had long-lasting organisational effects on the stress reactivity which prepared individuals for a risky future environment. Fish that were raised without older group members, had lower baseline cortisol concentrations and different expression patterns of stress receptors in the brain (Fig A). To examine the effects of nutritional state and stress exposure on behavioural flexibility, we manipulated the diet of adult fish, making some individuals lean and others well-fed, but not obese. We exposed these two groups to different levels of environmental stressors by showing them predators often or only occasionally. First, we measured their stress response towards a novel stressor in terms of how quickly their cortisol levels returned to normal levels. Second, we tested their behavioural flexibility in terms of the ability to learn a new task. We found effects on the short-term activation of the stress response: fish exposed to predators had a better stress response, with a quick return to normal cortisol levels (Fig. A), and were better at learning the new task. Interestingly, this result was even more pronounced in well-fed fish. This finding is consistent with the idea that repeated stress responses are costly for organisms and only well-nourished individuals can cope well with these costs. In another experiment, we blocked stress receptors in fish, preventing them from experiencing the effects of the stress hormones. These fish showed less flexibility in learning new routes and had stronger fear responses, directly demonstrating the importance of an appropriate stress response to flexibly cope with an environmental challenge. Our results have a wide range of implications for basic research as well animal husbandry. Overall, we show that mild stressors prepare individuals for future environmental challenges particularly when individuals are well-fed and not obese. In order to improve welfare and their ability to cope with stressors, it will thus be important to define the threshold between lean, well-fed and obese animals in captivity.