Response to environmental change in rainbow trout selected for divergent stress coping styles
Research Highlights
► Proactive rainbow trout show low flexibility and high level of routine formation. ► Reactive trout are more sensitive and readily respond to environmental changes. ► Differences in responsiveness may underlie other patterns of behavioural variation.
Introduction
An extensive literature on a variety of animal groups has documented the existence of consistent individual differences in behavioural and physiological responses to challenge [1], [2], [3], [4], [5]. Terms such as personality [6], [7], temperament [8] and coping styles [9], [10] have often been used to describe this phenomenon. Given the widespread incidence of consistent trait correlations, considerable research effort has been directed at elucidating the causes, development and function of such variation in responsiveness, as well as its significance for other biological disciplines [10], [11].
Individual variation in terms of specific behavioural patterns and correlations between them (or behavioural syndromes, [12]) has been characterised. Among other traits, the propensity of individuals to take risks of various kinds (i.e. boldness, [13]) and to attack rivals (i.e. aggressiveness, [14]) have been well studied. However, the behavioural differences concerned may include differences of a more general nature, including variation in sensitivity to any environmental change. The literature in variable stress coping styles, defined as “a coherent set of behavioural and physiological stress responses, which is consistent over time and characteristic to a certain group of individuals” [9] has thrown light on this topic, by identifying two broad patterns of response to challenge: the proactive coping strategy refers to a response that is physiologically characterised by low hypothalamus-pituitary-adrenal (HPA axis) reactivity and low parasympathetic reactivity, whereas sympathetic reactivity and testosterone activity is high. Behaviourally, proactive animals tend to show a fight–flight response and to be aggressive and bold [9], [10]. In contrast, animals with a reactive coping style show high HPA reactivity, high parasympathetic reactivity and low sympathetic reactivity and testosterone activity. The two strategies also differ in more general ways, in that reactive animals tend to be flexible whereas proactive animals are more rigid and tend to form and follow routines [9], [10], [14], [15], [16]. The existence of proactive and reactive phenotypes seems to be a widespread phenomenon, with some aspects of individual variation being reported in invertebrates (e.g. squids, Euprymna tasmanica, [4]), lizards (Anolis carolinensis, [17]) and in various species of fish (sticklebacks, Gasterosteus aculeatus [5], [18], [19]; the rainbow trout Oncorhynchus mykiss, [20], [21], [22]). Although coping strategies or behavioural syndromes are often interpreted as bimodal variables, individuals will often vary along a continuum with two extremes represented as tendencies. In this case, the proactive and the reactive coping strategies will represent the two extreme cases of the individual response to challenge present in the original population.
In this context, Wolf and collaborators [23] recently suggested that the existence and persistence of individual differences in response to challenge could be explained simply by the extent to which each individual perceive and react to environmental stimuli. According to this model, some individuals are highly sensitive to environmental change and readily modify their behaviour according to the prevailing conditions; in on other words they tend to be highly responsive and flexible. In contrast, others pay little attention to such changes, readily forming and following routines; such individuals are behaviourally unresponsive. Such differences in the way individuals appraise and process information about the environment may potentially play an important role in the expression and maintenance of individual variation in behaviour. To date, those differences have been characterised for only a few model species of birds [24] and mammals [14], [16], [25]. Comparative model species such as teleost fish have not been studied to address whether the association between coping style and behavioral flexibility versus routine formation is evolutionarily conserved. A better integration of controlled experimental manipulations with studies addressing ecological and evolutionary contexts would advance our understanding of the proximate mechanisms underlying individual differences in the response to environmental change. Therefore, the study described here was designed to look for discrepancies in responsiveness to environmental stimuli and routine formation in teleost fish expressing genetically mediated differences in coping style.
In fishes, knowledge of the physiological processes underlying behavioural responses to stress is growing, particularly for the rainbow trout (O. mykiss), which is the subject of the present study. In a selection programme that started in 1997 at the Centre for Ecology and Hydrology, Windermere, UK by Dr. T. G. Pottinger, adult fish from a commercial strain were selected for responsiveness to a standardized stressor (confinement) measured as levels of post-stress plasma cortisol [26], [27]. The selection programme created one high and one low responsive strain, hereafter referred to as the HR and LR strains respectively, showing that response to stress is a heritable trait in teleost fishes [26]. Physiological responsiveness is associated with distinctive behavioural patterns in trout; for example, in comparison to fish from the HR strain, LR fish are typically more likely to become dominant in dyadic contests and are bolder, in the sense of showing faster resumption of feeding after transfer to a novel environment [27], [28], [29], [30].
Although sensitive to specific environmental factors and experience such as nutritional status [31]; the pattern of behavioural, physiological and neurobiological responses shown by the LR/HR trout model is generally consistent with the proactive and reactive coping styles found in mammals and birds [2], [9], [10]. Therefore, this model was selected to determine whether fish with contrasting coping styles show differences in responsiveness to environmental change and in the formation of routines. This was accomplished by training individual HR and LR rainbow trout to find food in one arm of a T-maze, after which they were subjected to three different kinds of environmental change: relocation of food to the opposite arm of the maze, change of food location to the middle of the tank through which the fish passed in direction to the maze, and partial obstruction of this open area by a novel object. The performance of the HR and LR strains, in terms of the time it took fish to find and consume food was recorded in each condition.
Section snippets
The study fish
Eyed eggs from the 4th generation of high and low responding rainbow trout were transported from the Centre for Ecology and Hydrology, Windermere, UK to the Danish Institute of Fisheries Research, Hirtshals Denmark, where they where incubated, hatched and reared. We assumed these fish did not suffer the effects of transport and food restriction that affected adult fish transported to Norway [31], since the fish themselves were not subjected to transport as free-living individuals. In order to
Training period
In general, LR fish took more trials to start eating for the first time compared to HR fish (mean seconds ± S. E. HR = 26 ± 5; LR = 46 ± 7; t (18,2) = 2.45, p = 0.03). However, after the fish started eating, there were no strain differences in the number of trials to learn the foraging task (mean seconds ± S. E. HR = 8 ± 1; LR = 7 ± 1; t (18,2) = 0.69, p = 0.50).
Table 1 shows that during the feeding period following initial learning, and before any environmental manipulation took place, there were no differences between
Discussion
In this study, we examined routine strength and the response to environmental modification in HR and LR rainbow trout. These fish strains have been established as a model for the study of heritable variation in stress coping styles [21], [34], [35]. After fish from both strains had learnt to find localized food, striking differences between strains in the extent to which they followed the learned routines were observed, with HR fish finding and consuming relocated food much quicker than LR
Acknowledgements
We are thankful to T. Pottinger who created the HR and LR lines and provided the eggs, as well as for his helpful comments on an earlier version of this manuscript. We would also like to thank the Natural Environment Research Council of the United Kingdom for funding the establishment of the two strains. M. L. Ruiz-Gomez was funded by a scholarship from the Mexican Research Council CONACyT and the Universidad Autonoma del Estado de Mexico.
References (44)
- et al.
Consistency of temperament in bighorn ewes and correlates with behaviour and life history
Anim Behav
(2000) - et al.
Development of shy/bold behaviour in squid: context-specific phenotypes associated with developmental plasticity
Anim Behav
(2008) - et al.
Coping styles in animals: current status in behavior and stress-physiology
Neurosci Biobehav Rev
(1999) - et al.
The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease
Neurosci Biobehav Rev
(2005) - et al.
On the origin of allostasis and stress-induced pathology in farm animals: celebrating Darwin's legacy
Vet J
(2009) The relationship between anti-predator behaviour and aggression among conspecifics in the three-spined stickleback, Gasterosteus aculeatus
Anim Behav
(1976)- et al.
Stress and stress coping in fish, behavioural correlates and neuroendocrine mechanisms
Comp Biochem Phys
(2007) - et al.
Consistent individual differences in early exploratory behaviour of male great tits
Anim Behav
(1994) - et al.
Individual coping characteristics, rearing conditions and behavioural flexibility in pigs
Behav Brain Res
(2004) - et al.
Modification of the plasma cortisol response to stress in rainbow trout by selective breeding
Gen Comp Endocrinol
(1999)
Stress responsiveness affects dominant-subordinate relationships in rainbow trout
Horm Behav
Divergence in behavioural responses to stress in two strains of rainbow trout (Oncorhynchus mykiss) with contrasting stress responsiveness
Horm Behav
Serotonergic characteristics of rainbow trout divergent in stress responsiveness
Phys. Behav.
Behavioral plasticity in rainbow trout (Oncorhynchus mykiss) with divergent coping styles: when doves become hawks
Horm Behav
Hormonal correlates of environmentally induced metamorphosis in the western spadefoot toad, Scaphiopus hammondii
Gen Comp Endocrinol
Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates
Neurosci Biobehav Rev
Extinction of a conditioned response in rainbow trout selected for high or low responsiveness to stress
Horm Behav
Anxiety, cognition, and habit: a multiple memory systems perspective
Brain Res
The teleostean (zebrafish) dopaminergic system ascending to the subpallium (shiatum) is located in the basal diencephalon (posterior tuberculum)
Brain Res
The relation between dominance and exploratory behavior is context-dependent in wild great tits
Behav Ecol
A behavioural syndrome in the field cricket Gryllus integer: intrasexual aggression is correlated with activity in a novel environment
Biol J Linn Soc
Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus)
J Evol Biol
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