Fish can show emotional fever: stress-induced hyperthermia in zebrafish.

Whether fishes are sentient beings remains an unresolved and controversial question. Among characteristics thought to reflect a low level of sentience in fishes is an inability to show stress-induced hyperthermia (SIH), a transient rise in body temperature shown in response to a variety of stressors. This is a real fever response, so is often referred to as 'emotional fever'. It has been suggested that the capacity for emotional fever evolved only in amniotes (mammals, birds and reptiles), in association with the evolution of consciousness in these groups. According to this view, lack of emotional fever in fishes reflects a lack of consciousness. We report here on a study in which six zebrafish groups with access to a temperature gradient were either left as undisturbed controls or subjected to a short period of confinement. The results were striking: compared to controls, stressed zebrafish spent significantly more time at higher temperatures, achieving an estimated rise in body temperature of about 2-4°C. Thus, zebrafish clearly have the capacity to show emotional fever. While the link between emotion and consciousness is still debated, this finding removes a key argument for lack of consciousness in fishes.

A moving light stimulus elicits a sustained swimming response in farmed Atlantic salmon, Salmo salar L.

The productivity and welfare benefits of sustained swimming in fish are well documented, but are not yet exploited in commercial aquaculture. We report here on a study designed to test the feasibility of inducing sustained exercise in Atlantic salmon (Salmo salar L.) using a novel lighting device that provides an apparently moving light pattern. It was found that such a device could induce sustained swimming in Atlantic salmon held in tanks and that a centrally placed (inner ring) light system was far more effective in this context than one in which lights were placed on the outer wall of tanks. The central configuration was associated with enhanced rates of growth, feed conversion and reduced levels of plasma cortisol. Such developments in fish swimming technologies may assist the sustainability of finfish aquaculture through promotion of sustained exercise leading to improved productivity and welfare.

Response to environmental change in rainbow trout selected for divergent stress coping styles.

An extensive literature has documented differences in the way individual animals cope with environmental challenges and stressors. Two broad patterns of individual variability in behavioural and physiological stress responses are described as the proactive and reactive stress coping styles. In addition to variability in the stress response, contrasting coping styles may encompass a general difference in behavioural flexibility as opposed to routine formation in response to more subtle environmental changes and non-threatening novelties. In the present study two different manipulations, relocating food from a previously learned location, and introducing a novel object yielded contrasting responses in rainbow trout selected for high (HR) and low (LR) post stress plasma cortisol levels. No difference was seen in the rate of learning the original food location; however, proactive LR fish were markedly slower than reactive HR fish in altering their food seeking behaviour in response to relocated food. In contrast, LR fish largely ignored a novel object which disrupted feeding in HR fish. Hence, it appears that the two lines appraise environmental cues differently. This observation suggests that differences in responsiveness to environmental change are an integral component of heritable stress coping styles, which in this particular case, had opposite effects on foraging efficiency in different situations. Context dependent fitness effects may thus explain the persistence of stable divergence of this evolutionary widespread trait complex.

Behavioral and respiratory responses to stressors in multiple populations of three-spined sticklebacks that differ in predation pressure.

Individual animals of the same species inhabiting environments which differ in the frequency and magnitude of stressors often exhibit different physiological and behavioral responses to stressors. Here, we compare the respiratory response to confinement stress, and behavioral responses to ecologically relevant challenges among sticklebacks from 11 different populations varying in predation pressure. We found that sticklebacks from high predation populations breathed faster in response to confinement stress and were, on an average, more behaviorally responsive to a pike behind glass compared with sticklebacks from low predation populations. These patterns differ from the results of studies on other species, highlighting the need for a conceptual framework to understand the proximate and ultimate factors shaping variable responses to stressors over developmental and evolutionary time. Moreover, physiological and behavioral responses were integrated with each other, both at the individual and population levels. In general, fish that were more aggressive and bold in the presence of a predator breathed faster, independent of body size. These results are consistent with the growing body of evidence that individuals differ in a suite of physiological and behavioral mechanisms for coping with challenges in the environment.

Screening for coping style increases the power of gene expression studies.

BACKGROUND: Individuals of many vertebrate species show different stress coping styles and these have a striking influence on how gene expression shifts in response to a variety of challenges. PRINCIPAL FINDINGS: This is clearly illustrated by a study in which common carp displaying behavioural predictors of different coping styles (characterised by a proactive, adrenaline-based or a reactive, cortisol-based response) were subjected to inflammatory challenge and specific gene transcripts measured in individual brains. Proactive and reactive fish differed in baseline gene expression and also showed diametrically opposite responses to the challenge for 80% of the genes investigated. SIGNIFICANCE: Incorporating coping style as an explanatory variable can account for some the unexplained variation that is common in gene expression studies, can uncover important effects that would otherwise have passed unnoticed and greatly enhances the interpretive value of gene expression data.

Behavioral plasticity in rainbow trout (Oncorhynchus mykiss) with divergent coping styles: when doves become hawks.

Consistent and heritable individual differences in reaction to challenges, often referred to as stress coping styles, have been extensively documented in vertebrates. In fish, selection for divergent post-stress plasma cortisol levels in rainbow trout (Oncorhynchus mykiss) has yielded a low (LR) and a high responsive (HR) strain. A suite of behavioural traits is associated with this physiological difference, with LR (proactive) fish feeding more rapidly after transfer to a new environment and being socially dominant over HR (reactive) fish. Following transport from the UK to Norway, a switch in behavioural profile occurred in trout from the 3rd generation; HR fish regained feeding sooner than LR fish in a novel environment and became dominant in size-matched HR-LR pairs. One year after transport, HR fish still fed sooner, but no difference in social dominance was found. Among offspring of transported fish, no differences in feeding were observed, but as in pre-transported 3rd generation fish, HR fish lost fights for social dominance against size-matched LR opponents. Transported fish and their offspring retained their distinctive physiological profile throughout the study; HR fish showed consistently higher post-stress cortisol levels at all sampling points. Altered risk-taking and social dominance immediately after transport may be explained by the fact that HR fish lost more body mass during transport than did LR fish. These data demonstrate that some behavioural components of stress coping styles can be modified by experience, whereas behavioural plasticity is limited by genetic effects determining social position early in life story.

Social hierarchies, growth and brain serotonin metabolism in Atlantic salmon (Salmo salar) kept under commercial rearing conditions.

Monitoring social interactions between individuals in large, high-density groups poses several challenges. Here we demonstrate that relative concentrations of serotonin (5-Hydroxytryptamine, 5-HT) and its principal catabolite 5-Hydroxyindoleacetic acid (5-HIAA) in brain tissue of individual fish reflect social organisation in large groups of farmed Atlantic salmon. In the central nervous system of vertebrates, the monoamine neurotransmitter/neuromodulator 5-HT is critical for maintaining adaptive physiological, cognitive and emotional processes. In both teleost fish and mammals it has previously been shown that social interactions in small groups lead to elevated 5-HT release and/or metabolism in subordinate individuals, as indicated by the 5-HIAA/5-HT concentration ratio. In the current study, evidence is presented of non-linear dominance hierarchies in farmed Atlantic salmon (Salmo salar) kept at high rearing densities. The physiological effect of these hierarchies was decreased when food resources were abundant, although some subordinate fish still showed altered brain serotonergic activity and failed to grow even feed was available in excess. The largest effect of decreased feed rations was seen in fish of intermediate size, where competition appeared to increase with reduced access to feed. The largest individuals in each rearing unit showed low 5-HIAA/5-HT ratios independent of feeding regime. A novel observation, with respect to previous studies, was that elevated brain 5-HIAA/5-HT ratios resulted from decreased 5-HT concentrations rather than elevated 5-HIAA in small fish. Thus, in light of the serotonin deficit hypothesis of depression, it cannot be excluded that social stress is important for animal welfare even in large, relatively homogenous groups of animals reared in captivity.

Parallel evolution of Pitx1 underlies pelvic reduction in Scottish threespine stickleback (Gasterosteus aculeatus).

Little is known about the genetic and molecular mechanisms that underlie adaptive phenotypic variation in natural populations or whether similar genetic and molecular mechanisms are utilized when similar adaptive phenotypes arise in independent populations. The threespine stickleback (Gasterosteus aculeatus) is a good model system to investigate these questions because these fish display a large amount of adaptive phenotypic variation, and similar adaptive phenotypes have arisen in multiple, independent stickleback populations. A particularly striking pattern of parallel evolution in sticklebacks is reduction of skeletal armor, which has occurred in numerous freshwater locations around the world. New genetic and genomic tools for the threespine stickleback have made it possible to identify genes that underlie loss of different elements of the skeletal armor. Previous work has shown that regulatory mutations at the Pitx1 locus are likely responsible for loss of the pelvic structures in independent stickleback populations from North America and Iceland. Here we show that the Pitx1 locus is also likely to underlie pelvic reduction in a Scottish population of threespine stickleback, which has apparently evolved pelvic reduction under a different selection regime than the North American populations.

Variable neuroendocrine responses to ecologically-relevant challenges in sticklebacks.

Variable neuroendocrine responses to ecologically-relevant challenges in sticklebacks. PHYSIOL BEHAV 00(0) 000-000, 2006. Here, we compare the behavioral, endocrine and neuroendocrine responses of individual sticklebacks exposed to either an unfamiliar conspecific or to a predator. We found that the two stressors elicited a similar hypothalamic-pituitary-interrenal response as assessed by whole-body concentrations of cortisol, but produced quite different patterns of change in brain monoamine and monoamine metabolite content as assessed by concentrations of serotonin (5-HT), dopamine (DA), norepinephrine (NE) and the monoamine metabolites 5-hydroxyindole acetic acid (5-HIAA), homovanillic acid (HVA) and 3-4-dihydroxyphenylacetic acid (DOPAC). For example, relative to baseline levels, NE levels were elevated in individuals exposed to a predator but were lower in individuals confronted by a challenging conspecific. Levels of monoamine neurotransmitters in specific regions of the brain showed extremely close links with behavioral characteristics. Frequency of attacking a conspecific and inspecting a predator were both positively correlated with concentrations of NE. However, whereas serotonin was negatively correlated with frequency of attacking a conspecific, it was positively associated with predator inspection. The data indicate that the qualitative and quantitative nature of the neuroendocrine stress response of sticklebacks varies according to the nature of the stressor, and that interindividual variation in behavioural responses to challenge are reflected by neuroendocrine differences.

Using the functional response to determine the nature of unequal interference among foragers.

The food intake rate of foragers may be reduced as a result of interference, which may be asymmetric among individuals and occur as a result of intimidation, direct aggression or filtering. It is important to distinguish among these types of interference, because each can have different consequences for individuals, foraging groups and populations. We demonstrate the application of the functional response as a tool for distinguishing between types of interference. We apply the approach to juvenile Atlantic salmon and show that stepwise elimination of interference types is possible from regression analyses of functional responses, identifying filtering as the only effective type of interference in the study environment.

Female sex pheromone-mediated effects on behavior and consequences of male competition in the shore crab (Carcinus maenas).

Exposure to receptive female pheromone elicits guarding behavior in shore crab males (Carcinus maenas), but little is known about the effects of sex pheromone on male competition or if the female plays an active role in mate choice. This study examined whether female pheromone enhanced agonistic behavior between males and what effects visual and chemical cues had on the rules and costs of such contests. We also investigated whether females exhibit a preference for males in terms of size. Under laboratory conditions, solitary male shore crabs engaged males who already had possession of a female. The visual and chemical presence of a receptive female had an impact on contest rules and costs. Fights were costly in terms of duration and of sustaining injury with either one or both crabs incurring injury in 40% of fights. To investigate the metabolic consequences of fighting over a perceived sexual resource (chemical cue only), fights were staged between pairs of size-matched males in the presence of water containing the female sex pheromone, water in which males had been kept, and untreated seawater. The duration and intensity of contests were greater when staged in the presence of the female pheromone compared with the two other treatments. Crabs that fought in the presence of female sex pheromone also had a greater accumulation of L-lactate and a reduction of glycogen stores. Fights were less costly in terms of injury with a single chemical cue compared with enhanced costs with a multiple sexual cue. The importance of female choice was determined by presenting postmolt females with different sized males. Males were kept in a fixed position, and the majority of females approached and performed courtship behavior to the largest males, demonstrating that females may be selective in terms of size.