Correlated behaviour and stress physiology in fish exposed to different levels of predation pressure

Abstract

Summary1. Natural selection can generate correlated suites of phenotypic traits by acting independently on physiological and behavioural characters or on mechanisms that exert pleiotropic actions. 2. Current theory, supported by artificial selection studies, suggests that physiological and behavioural stress responses are at least partially under genetic control and covary in a predictable manner. Indeed, physiological mechanisms such as hormonal stress responsiveness may underlie variation in behaviour, including consistent behaviours described as temperament or personality, with bolder, more exploratory and active individuals being less hormonally responsive to stressors. 3. This relationship, however, has yet to be demonstrated in natural populations. We investigated the relationship between hormonal and behavioural stress responsiveness in multiple natural populations of a tropical freshwater poeciliid fish, Brachyrhaphis episcopi, that experience different levels of predation pressure and hence encounter different rates of stressful events. Predation can impose a strong selection pressure, and living with a high risk of predation is known to select for specific behavioural traits. 4. We quantified variation in stress responsiveness via cortisol release rates (exp. 1) and behaviour in an open field test followed by cortisol release rates (exp. 2). Populations exposed to high levels of predation were consistently more exploratory and active and had lower release rates of cortisol in response to a stressor than conspecifics sampled at sites with few predators. 5. However, this difference in stress responsiveness was only apparent after fish had experienced the mild stress of behaviour testing (in exp. 2), which resulted in elevation of cortisol levels. The relationship between hormone release and behaviour was also not apparent within populations once independent factors were controlled for, highlighting the importance of factors such as size and sex on individual variability. 6. This study demonstrates that the relationship between hormonal and behavioural stress responsiveness can result from natural selection pressures, such as that imposed by predation.

Predators inhibit brain cell proliferation in natural populations of electric fish, Brachyhypopomus occidentalis

“…However, under laboratory circumstances, animals lack many of the behavioural options to respond to predators, and given that the perception of control is a prime determinant of the stress response [2], the relevance of these studies to naturally occurring glucocorticoid secretion is not clear. Indeed, in the few cases in which fish from field populations were examined, those living among abundant predators had lower cortisol production and reduced stress responses compared with fish in low-predation environments [20,44]. We found that basal and stress-induced cortisol levels were unrelated to predator exposure and tail injury, indicating that B. occidentalis regulate their glucocorticoid levels independently of predator stimuli.…”

“…In the presence of abundant predators, prey probably move more cautiously and in a more limited range [13,23,43] (however, see [44]). Thus, predators could influence prey by directly influencing the brain through the 'physiology of fear' (e.g.…”

Covariation between behaviour and physiology indicators of coping style in zebrafish (Danio rerio)

“…Consequently, stress may reduce reproductive success (Schreck et al 2001) and disrupt trophic interactions (Archard et al 2012), from which it follows that stress may not only negatively affect individuals but also contribute to population decline and the possible extinction of species (Schaaf et al 2008). Nevertheless, natural populations typically consist of individuals of a range of different copying styles and such a mixture means that individuals will vary in how well they fare under stressful situations but also provides a population with some flexibility to persist (Koolhaas et al 1999, Korte et al 2005.…”

Phenotypic differences between the sexes in the sexually plastic mangrove rivulus fish (Kryptolebias marmoratus)

“…Risk taking was assayed using an emergence from shelter/openfield exploration paradigm (e.g. Archard et al, 2012). Individuals were acclimated for 2 h beginning at 10:00 h in an enclosure constructed from opaque black corrugated plastic.…”