Growth-enhanced salmon modify stream ecosystem functioning.

Use of fast-growing domesticated and/or genetically modified strains of fish is becoming increasingly common in aquaculture, increasing the likelihood of deliberate or accidental introductions into the wild. To date, their ecological impacts on ecosystems remain to be quantified. Here, using a controlled phenotype manipulation by implanting growth hormone in juvenile Atlantic salmon (Salmo salar), we found that growth-enhanced fish display changes in several phenotypic traits known to be important for ecosystem functioning, such as habitat use, morphology and excretion rate. Furthermore, these phenotypic changes were associated with significant impacts on the invertebrate community and key stream ecosystem functions such as primary production and leaf-litter decomposition. These findings provide novel evidence that introductions of growth-enhanced fish into the wild can affect the functioning of natural ecosystems and represent a form of intraspecific invasion. Consequently, environmental impact assessments of growth-enhanced organisms need to explicitly consider ecosystem-level effects.

High risk no gain-metabolic performance of hatchery reared Atlantic salmon smolts, effects of nest emergence time, hypoxia avoidance behaviour and size.

When animals are reared for conservational releases it is paramount to avoid reducing genetic and phenotypic variation over time. This requires an understanding of how diverging behavioural and physiological traits affect performance both in captivity and after release. In Atlantic salmon, emergence time from the spawning gravel has been linked to certain behavioural and physiological characteristics and to the concept of stress coping styles. Early emerging fry has for example been shown to be bolder and more aggressive and to have higher standard metabolic rates compared to late emerging fry. The first aim was therefore to examine if emergence latency affect the behavioural stress coping response also beyond the fry and parr stage. This was done using a hypoxia avoidance test, where an active behavioural avoidance response can be related to higher risk taking. No behavioural differences were found between the two emergence fractions either at the parr or pre-smolt stage, instead smaller individuals were more prone to express an "active" hypoxia avoidance response. Further, an individual expressing a "passive" response as parr were also more prone to express this behaviour at the pre-smolt stage. While there are some previous studies showing that early emerging individuals with a bolder personality may be favored within a hatchery setting it is not known to what extent these early differences persist to affect performance after release. The second aim was therefore to compare the physiological performance at the time of release as smolts using the two subgroups; 1) early emerging fish showing active hypoxia avoidance (Early+Bold) and 2) late emerging fish showing a passive hypoxia response (Late+Shy). The Early+Bold group showed a higher red blood cell swelling, suggesting a higher adrenergic output during stress, whereas there was no difference in post-stress plasma cortisol or physiological smolt status. While there was no difference in standard metabolic rate between the groups, the Early+Bold group exhibited a lower maximum metabolic rate and aerobic scope following strenuous swimming. In captivity this may have no clear negative effects, but in the wild, a more risk prone behavioural profile linked to a lower aerobic capacity to escape from e.g. a predator attack, could clearly be disadvantageous.

Inactive trout come out at night: behavioral variation, circadian activity, and fitness in the wild.

Theory suggests that high activity levels in animals increase growth at the cost of increased mortality. This growth-mortality tradeoff has recently been incorporated into the wider framework of the pace-of-life syndrome (POLS) hypothesis. However, activity is often quantified only in the laboratory and on a diurnal basis, leaving open the possibility that animals manage predation risk and feeding efficiency in the wild by modulating their circadian activity rhythms. Here we investigate how laboratory activity in wild brown trout parr (Salmo trutta L.) associates with circadian activity, growth, and mortality in their natal stream. We found that individuals with high activity in the laboratory displayed high dispersal and cathemeral activity in their natal stream. In contrast, trout with low laboratory activity showed variation of activity in the wild, which was negatively related to the light intensity. Our results do not support the growth-mortality trade-off of the POLS hypothesis as highly active, fast-growing individuals showed higher survival than inactive conspecifics. These novel results show for the first time that active and inactive individuals, as scored in the lab, can show different circadian patterns of behavior in the wild driven by light intensity. This implies that studies conducted under a narrow range of light conditions can bias our understanding of individual behavioral variation and its fitness consequences in the wild.

State-dependent behavior and alternative behavioral strategies in brown trout (Salmo trutta L.) fry.

ABSTRACT: Animals generally adjust their behavior in response to bodily state (e.g., size and energy reserves) to optimize energy intake in relation to mortality risk, weighing predation probability against the risk of starvation. Here, we investigated whether brown trout Salmo trutta adjust their behavior in relation to energetic status and body size during a major early-life selection bottleneck, when fast growth is important. Over two consecutive time periods (P1 and P2; 12 and 23 days, respectively), food availability was manipulated, using four different combinations of high (H) and low (L) rations (i.e., HH, HL, LH, and LL; first and second letter denoting ration during P1 and P2, respectively). Social effects were excluded through individual isolation. Following the treatment periods, fish in the HL treatment were on average 15-21 % more active than the other groups in a forced open-field test, but large within-treatment variation provided only weak statistical support for this effect. Furthermore, fish on L-ration during P2 tended to be more actively aggressive towards their mirror image than fish on H-ration. Body size was related to behavioral expression, with larger fish being more active and aggressive. Swimming activity and active aggression were positively correlated, forming a behavioral syndrome in the studied population. Based on these behavioral traits, we could also distinguish two behavioral clusters: one consisting of more active and aggressive individuals and the other consisting of less active and aggressive individuals. This indicates that brown trout fry adopt distinct behavioral strategies early in life. SIGNIFICANCE STATEMENT: This paper provides information on the state-dependence of behavior in animals, in particular young brown trout. On the one hand, our data suggest a weak energetic state feedback where activity and aggression is increased as a response to short term food restriction. This suggests a limited scope for behavioral alterations in the face of starvation. On the other hand, body size is linked to higher activity and aggression, likely as a positive feedback between size and dominance. The experiment was carried out during the main population survival bottleneck, and the results indicate that growth is important during this stage, as 1) behavioral compensation to increase growth is limited, and 2) growth likely increases the competitive ability. However, our data also suggests that the population separates into two clusters, based on combined scores of activity and aggression (which are positively linked within individuals). Thus, apart from an active and aggressive strategy, there seems to be another more passive behavioral strategy.

Telomere length covaries with personality in wild brown trout.

The prevalence of consistent among-individual differences in behaviour, or personality, makes adaptive sense if individuals differ in stable state variables that shift the balance between the costs and benefits of their behavioural decisions. These differences may give rise to both individual differences in, and covariance among, behaviours that influence an individual's exposure to risks. We here study the link between behaviour and a candidate state variable previously overlooked in the study of state-dependent personality variation: telomere length. Telomeres are the protective endcaps of chromosomes and their erosion with age is thought to play a crucial role in regulating organismal senescence and intrinsic lifespan. Following evidence that shorter telomeres may reduce the lifespan of animals in a wide range of taxa, we predict individuals with shorter telomeres to behave more boldly and aggressively. In order to test this, we measured telomere length and behaviour in wild juvenile brown trout (Salmo trutta). We found individuals with shorter fin telomeres to behave consistently more boldly and aggressively under controlled conditions in the laboratory. No such relationship was found with muscle telomere length 3-4months after the behavioural assays. We suggest that telomere dynamics are an important factor integrating personality traits with other state variables thought to be important in the regulation of behaviour, such as metabolism, disease resistance and growth.

Sight or smell? Behavioural and heart rate responses in subordinate rainbow trout exposed to cues from dominant fish.

Many animals, including fish, can utilize both vision and the chemical senses in intra-specific communication. However, the relative influence of these sensory modalities on behavioral and physiological responses in social interactions is not well understood. The aim of this study was therefore to investigate the relative effects of visual and chemical stimuli from dominant individuals on the behavioral and physiological responses of subordinate rainbow trout (Oncorhynchus mykiss). External electrodes were used to detect ECG signals from free-swimming fish. This method allowed the simultaneous recording of behavioral and physiological responses, and possible sex differences in these responses were also investigated. The results suggest that, in this context, visual cues are more important than chemical cues in settling the social hierarchy in rainbow trout because a combination of chemical and visual exposure generally yielded a response in focal fish that was similar to the response elicited by visual exposure alone. Both activity and physiological responses were most pronounced during the first ten seconds after exposure, with subordinate fish moving closer to the dominant, accompanied by a strong bradycardic response. Furthermore, females acted more boldly and moved closer to the dominant fish than males, but here the effect of the modes was additive, with a stronger effect of the combined visual and chemical exposure. Overall, the extra information furnished to the fish in the form of chemical cues did not change either the behavioral or the physiological response. This result suggests that visual cues are more important than chemically mediated ones for social communication and individual recognition in rainbow trout.

Rapid growth accelerates telomere attrition in a transgenic fish.

BACKGROUND: Individuals rarely grow as fast as their physiologies permit despite the fitness advantages of being large. One reason may be that rapid growth is costly, resulting for example in somatic damage. The chromosomal ends, the telomeres, are particularly vulnerable to such damage, and telomere attrition thus influences the rate of ageing. Here, we used a transgenic salmon model with an artificially increased growth rate to test the hypothesis that rapid growth is traded off against the ability to maintain somatic health, assessed as telomere attrition. RESULTS: We found substantial telomere attrition in transgenic fish, while maternal half-sibs growing at a lower, wild-type rate seemed better able to maintain the length of their telomeres during the same time period. CONCLUSIONS: Our results are consistent with a trade-off between rapid growth and somatic (telomere) maintenance in growth-manipulated fish. Since telomere erosion reflects cellular ageing, our findings also support theories of ageing postulating that unrepaired somatic damage is associated with senescence.

Effects of emergence time and early social rearing environment on behaviour of Atlantic salmon: consequences for juvenile fitness and smolt migration.

Consistent individual differences in behaviour have been well documented in a variety of animal taxa, but surprisingly little is known about the fitness and life-history consequences of such individual variation. In wild salmonids, the timing of fry emergence from gravel spawning nests has been suggested to be coupled with individual behavioural traits. Here, we further investigate the link between timing of spawning nest emergence and behaviour of Atlantic salmon (Salmo salar), test effects of social rearing environment on behavioural traits in fish with different emergence times, and assess whether behavioural traits measured in the laboratory predict growth, survival, and migration status in the wild. Atlantic salmon fry were sorted with respect to emergence time from artificial spawning nest into three groups: early, intermediate, and late. These emergence groups were hatchery-reared separately or in co-culture for four months to test effects of social rearing environment on behavioural traits. Twenty fish from each of the six treatment groups were then subjected to three individual-based behavioural tests: basal locomotor activity, boldness, and escape response. Following behavioural characterization, the fish were released into a near-natural experimental stream. Results showed differences in escape behaviour between emergence groups in a net restraining test, but the social rearing environment did not affect individual behavioural expression. Emergence time and social environment had no significant effects on survival, growth, and migration status in the stream, although migration propensity was 1.4 to 1.9 times higher for early emerging individuals that were reared separately. In addition, despite individuals showing considerable variation in behaviour across treatment groups, this was not translated into differences in growth, survival, and migration status. Hence, our study adds to the view that fitness (i.e., growth and survival) and life-history predictions from laboratory measures of behaviour should be made with caution and ideally tested in nature.

Telomere dynamics in wild brown trout: effects of compensatory growth and early growth investment.

After a period of food deprivation, animals often respond with a period of faster than normal growth. Such responses have been suggested to result in decreased chromosomal maintenance, which in turn may affect the future fitness of an individual. Here, we present a field experiment in which a food deprivation period of 24 days was enforced on fish from a natural population of juvenile brown trout (Salmo trutta) at the start of the high-growth season in spring. The growth of the food-deprived fish and a non-deprived control group was then monitored in the wild during 1 year. Fin tissue samples were taken at the start of the experiment and 1 year after food deprivation to monitor the telomere dynamics, using reduced telomere length as an indicator of maintenance cost. The food-deprived fish showed partial compensatory growth in both mass and length relative to the control group. However, we found no treatment effects on telomere dynamics, suggesting that growth-compensating brown trout juveniles are able to maintain their telomeres during their second year in the stream. However, body size at the start of the experiment, reflecting growth rate during their first year of life, was negatively correlated with change in telomere length over the following year. This result raises the possibility that rapid growth early in life induces delayed costs in cellular maintenance.

Ghrelin increases food intake, swimming activity and growth in juvenile brown trout (Salmo trutta).

Several key functions of ghrelin are well conserved through vertebrate phylogeny. However, some of ghrelin's effects are contradictory and among teleosts only a limited number of species have been used in functional studies on food intake and foraging-related behaviors. Here we investigated the long-term effects of ghrelin on food intake, growth, swimming activity and aggressive contest behavior in one year old wild brown trout (Salmo trutta) using intraperitoneal implants. Food intake and swimming activity were individually recorded starting from day 1, and aggressive behavior was tested at day 11, after ghrelin implantation. Body weight and growth rate were measured from the beginning to the end of the experiment. Triglycerides and lipase activity in muscle and liver; monoaminergic activity in the telencephalon and brainstem; and neuropeptide Y (NPY) mRNA levels in the hypothalamus were analyzed. Ghrelin treatment was found to increase food intake and growth without modifying lipid deposition or lipid metabolism in liver and muscle. Ghrelin treatment led to an increased foraging activity and a trend towards a higher swimming activity. Moreover, ghrelin-treated fish showed a tendency to initiate more conflicts, but this motivation was not reflected in a higher ability to win the conflicts. No changes were observed in monoaminergic activity and NPY mRNA levels in the brain. Ghrelin is therefore suggested to act as an orexigenic hormone regulating behavior in juvenile wild brown trout. These actions are accompanied with an increased growth without the alteration of liver and muscle lipid metabolism and they do not seem to be mediated by changes in brain monoaminergic activity or hypothalamic expression of NPY.

Modes of competition: adding and removing brown trout in the wild to understand the mechanisms of density-dependence.

While the prevalence of density-dependence is well-established in population ecology, few field studies have investigated its underlying mechanisms and their relative population-level importance. Here, we address these issues, and more specifically, how differences in body-size influence population regulation. For this purpose, two experiments were performed in a small coastal stream on the Swedish west coast, using juvenile brown trout (Salmo trutta) as a study species. We manipulated densities of large and small individuals, and observed effects on survival, migration, condition and individual growth rate in a target group of intermediate-sized individuals. The generality of the response was investigated by reducing population densities below and increasing above the natural levels (removing and adding large and small individuals). Reducing the density (relaxing the intensity of competition) had no influence on the response variables, suggesting that stream productivity was not a limiting factor at natural population density. Addition of large individuals resulted in a negative density-dependent response, while no effect was detected when adding small individuals or when maintaining the natural population structure. We found that the density-dependent response was revealed as reduced growth rate rather than increased mortality and movement, an effect that may arise from exclusion to suboptimal habitats or increased stress levels among inferior individuals. Our findings confirm the notion of interference competition as the primary mode of competition in juvenile salmonids, and also show that the feedback-mechanisms of density-dependence are primarily acting when increasing densities above their natural levels.

Density-dependent compensatory growth in brown trout (Salmo trutta) in nature.

Density-dependence is a major ecological mechanism that is known to limit individual growth. To examine if compensatory growth (unusually rapid growth following a period of imposed slow growth) in nature is density-dependent, one-year-old brown trout (Salmo trutta L.) were first starved in the laboratory, and then released back into their natural stream, either at natural or at experimentally increased population density. The experimental trout were captured three times over a one-year period. We found no differences in growth, within the first month after release (May-June), between the starved fish and the control group (i.e. no evidence of compensation). During the summer however (July-September), the starved fish grew more than the control group (i.e. compensation), and the starved fish released into the stream at a higher density, grew less than those released at a natural density, both in terms of weight and length (i.e. density-dependent compensation). Over the winter (October-April), there were no effects of either starvation or density on weight and length growth. After the winter, starved fish released at either density had caught up with control fish in body size, but recapture rates (proxy for survival) did not indicate any costs of compensation. Our results suggest that compensatory growth in nature can be density-dependent. Thus, this is the first study to demonstrate the presence of ecological restrictions on the compensatory growth response in free-ranging animals.

Metabolic scope and interspecific competition in sculpins of Greenland are influenced by increased temperatures due to climate change.

Ongoing climate change has led to an increase in sea surface temperatures of 2-4°C on the west coast of Greenland. Since fish are ectothermic, metabolic rate increases with ambient temperature. This makes these animals particularly sensitive to changes in temperature; subsequently any change may influence their metabolic scope, i.e. the physiological capacity to undertake aerobically challenging activities. Any temperature increase may thus disrupt species-specific temperature adaptations, at both the molecular level as well as in behavior, and concomitant species differences in the temperature sensitivity may shift the competitive balance among coexisting species. We investigated the influence of temperature on metabolic scope and competitive ability in three species of marine sculpin that coexist in Greenland coastal waters. Since these species have different distribution ranges, we hypothesized that there should be a difference in their physiological response to temperature; hence we compared their metabolic scope at three temperatures (4, 9 and 14°C). Their competitive ability at the ambient temperature of 9°C was also tested in an attempt to link physiological capacity with behaviour. The Arctic staghorn sculpin, the species with the northernmost distribution range, had a lower metabolic scope in the higher temperature range compared to the other two species, which had similar metabolic scope at the three temperatures. The Arctic staghorn sculpin also had reduced competitive ability at 9°C and may thus already be negatively affected by the current ocean warming. Our results suggest that climate change can have effects on fish physiology and interspecific competition, which may alter the species composition of the Arctic fish fauna.

Natural selection, plasticity and the emergence of a behavioural syndrome in the wild.

Individuals often show consistent behavioural differences where behaviours can form integrated units across functionally different contexts. However, the factors causing and maintaining behavioural syndromes in natural populations remain poorly understood. In this study, we provide evidence for the emergence of a behavioural syndrome during the first months of life in wild brown trout (Salmo trutta). Behavioural traits of trout were scored before and after a 2-month interval covering a major survival bottleneck, whereupon the consistency and covariance of behaviours were analysed. We found that selection favoured individuals with high activity levels in an open-field context, a personality trait consistent throughout the duration of the experiment. In addition, a behavioural syndrome emerged over the 2 months in the wild, linking activity to aggressiveness and exploration tendency. These novel results suggest that behavioural syndromes can emerge rapidly in nature from interaction between natural selection and behavioural plasticity affecting single behaviours.

Oxidative stress in growth hormone transgenic coho salmon with compressed lifespan--a model for addressing aging.

Growth hormone (GH) transgenic fish have dramatically enhanced growth rates, increased oxygen demands and reactive oxygen species production. GH-transgenic coho salmon provide an opportunity to address effects of increased metabolism on physiological aging. The objective of this study was to compare oxidative stress in wild-type (WT) and GH-transgenic (T) coho salmon (Oncorhynchus kisutch) of different ages (1 and 2 years). Antioxidant enzyme activity, protein carbonyls (PC) and glutathione (GSH, GSSG) were measured. PC correlated to growth rates in individual fish. T fish exhibited lower antioxidant enzyme activities and GSH levels compared to the WT, while levels of PC and GSSG were higher. Age affects were observed in both WT and T fish; enzyme activities and GSH decreased while PC and GSSG increased. Our results support the metabolic rate theory of aging. This study aims to be a platform for continued studies of the theories of aging using fish as model organisms.

Does waterborne citalopram affect the aggressive and sexual behaviour of rainbow trout and guppy?

Citalopram is one of several selective serotonin reuptake inhibitors (SSRIs) commonly found in treated sewage effluents. Accordingly, there are concerns about possible adverse effects of SSRIs on aquatic organisms, particularly behavioural effects similar to those associated with SSRI use in humans. Rainbow trout fry and adult male guppies were therefore exposed to waterborne citalopram, ranging from environmentally relevant to high concentrations (1, 10, 100 µg/L) for 3-7 days. Under these experimental conditions citalopram does not appear to cause significant effects on aggression in rainbow trout fry or on sexual behaviour in male guppies. This may be explained by a relatively low uptake of citalopram from water to fish.

The cost of catching up: increased winter mortality following structural growth compensation in the wild.

Although laboratory and observational studies suggest that many animals are capable of compensatory growth after periods of food shortage, few field experiments have demonstrated structural growth compensation in the wild. Here, we addressed the hypotheses that (i) food restriction can induce structural compensatory growth in free-living animals, (ii) that compensation is proportional to the level of body size retardation and (iii) that compensation induces mortality costs. To test these, wild brown trout (Salmo trutta) yearlings were brought to the lab, tagged individually, subjected to four levels of food deprivation (including a control), released back into the native stream and recaptured after one, five and ten months. Brown trout fully restored condition and partially restored mass within a month, whereas compensation in structure (i.e. body length) was not evident until after five months, supporting hypothesis 1. As the level of growth compensation was similar among the three deprived groups, hypothesis 2 was not supported. A final recapture after winter revealed delayed mortality, apparently induced by the compensatory response in the deprived groups, which is consistent with hypothesis 3. To our knowledge, this is the first field experiment demonstrating structural compensatory growth and associated costs in a wild animal population.

Growth hormone transgenic salmon pay for growth potential with increased predation mortality.

Recent advances in gene technology have been applied to create fast-growing transgenic fish, which are of great commercial interest owing to their potential to shorten production cycles and increase food production. However, there is growing concern and speculation over the impact that escaped growth hormone (GH)-transgenic fish may have on the natural environment. To predict these risks it is crucial to obtain empirical data on the relative fitness of transgenic and non-transgenic fish under nature-like conditions. Using landscaped stream aquaria with live food and predators, we show that the predation mortality of newly hatched GH-transgenic coho salmon fry (Oncorhynchus kisutch) is much higher than in non-transgenic conspecifics, and that this difference is amplified when food abundance decreases. The growth rate of transgenic and non-transgenic fish is similar at high food levels, whereas transgenic fish grow more slowly than non-transgenic fish when food abundance is reduced. Our results suggest that the fitness of young GH-transgenic coho salmon in the wild will be determined by both predation pressure and food availability.