Variation in phenotypic plasticity across age-at-maturity genotypes in wild Atlantic salmon.

Evolution of phenotypic plasticity requires genotype-environment interaction. The discovery of two large-effect loci in the vgll3 and six6 genomic regions associated with the number of years the Atlantic salmon spend feeding at sea before maturation (sea age), provides a unique opportunity to study evolutionary potential of phenotypic plasticity. Using data on 1246 Atlantic salmon caught in the River Surna in Norway, we show that variation in mean sea age among years (smolt cohorts 2013-2018) is influenced by genotype frequencies as well as interaction effects between genotype and year. Genotype-year interactions suggest that genotypes may differ in their response to environmental variation across years, implying genetic variation in phenotypic plasticity. Our results also imply that plasticity in sea age will evolve as an indirect response to selection on mean sea age due to a shared genetic basis. Furthermore, we demonstrate differences between years in the additive and dominance functional genetic effects of vgll3 and six6 on sea age, suggesting that evolutionary responses will vary across environments. Considering the importance of age at maturity for survival and reproduction, genotype-environment interactions likely play an important role in local adaptation and population demography in Atlantic salmon.

Ecological regime shift in the Northeast Atlantic Ocean revealed from the unprecedented reduction in marine growth of Atlantic salmon.

Ecological regime shifts are abrupt changes in the structure and function of ecosystems that persist over time, but evidence of contemporary regime shifts are rare. Historical scale data from 52,384 individual wild Atlantic salmon caught in 180 rivers from 1989 to 2017 reveal that growth of Atlantic salmon across the Northeast Atlantic Ocean abruptly decreased following the year 2004. At the same time, the proportion of early maturing Atlantic salmon decreased. These changes occurred after a marked decrease in the extent of Arctic water in the Norwegian Sea, a subsequent warming of spring water temperature before Atlantic salmon entering the sea, and an approximately 50% reduction of zooplankton across large geographic areas of the Northeast Atlantic Ocean. A sudden decrease in growth was also observed among Atlantic mackerel in the Norwegian Sea. Our results point toward an ecosystem-scale regime shift in the Northeast Atlantic Ocean.

Selection against individuals from genetic introgression of escaped farmed salmon in a natural population of Atlantic salmon.

The viability of wild Atlantic salmon populations is threatened by genetic introgression from escaped farmed salmon. Farmed Atlantic salmon are genetically improved for important commercial traits and a life in captivity but are poorly adapted to the natural environment. The rate of gene flow from escaped farmed to wild salmon depends on their spawning success and on offspring survival at various life stages. We here investigate relative survival of introgressed juvenile Atlantic salmon (parr) in a river in northern Norway. The studied population has experienced genetic introgression from farmed salmon for about four generations (20 years). We followed two cohorts of parr from the year of hatching (0+) to the age of 2 years (2+). Farmed genetic introgression was quantified at the individual level and on a continuous scale using diagnostic SNPs. Population-level genetic introgression decreased from 0+ to 2+ by 64% (2011 cohort) and 37% (2013 cohort). This change was driven by a 70% (2011 cohort) and 49% (2013 cohort) lower survival from age 0+ to 2+ in introgressed parr compared to parr of wild origin. Our observations show that there is natural selection against genetic introgression with a potential cost of lower productivity.

Can variation in standard metabolic rate explain context-dependent performance of farmed Atlantic salmon offspring?

Escaped farmed Atlantic salmon interbreed with wild Atlantic salmon, leaving offspring that often have lower success in nature than pure wild salmon. On top of this, presence of farmed salmon descendants can impair production of wild-type recruits. We hypothesize that both these effects connect with farmed salmon having acquired higher standard metabolic rates (SMR, the energetic cost of self-maintenance) during domestication. Fitness-related advantages of phenotypic traits associated with both high SMR and farmed salmon (e.g., social dominance) depend on environmental conditions, such as food availability. We hypothesize that farmed offspring have an advantage at high food availability due to, for example, dominance behavior but suffer increased risks of starvation when food is scarce because this behavior is energy-demanding. To test these hypotheses, we first compare embryo SMR of pure farmed, farmed-wild hybrids and pure wild offspring. Next, we test early-life performance (in terms of survival and growth) of hybrids relative to that of their wild half-siblings, as well as their competitive abilities, in semi-natural conditions of high and low food availability. Finally, we test how SMR affects early-life performance at high and low food availability. We find inconclusive support for the hypothesis that domestication has induced increased SMR. Further, wild and hybrid juveniles had similar survival and growth in the semi-natural streams. Yet, the presence of hybrids led to decreased survival of their wild half-siblings. Contrary to our hypothesis about context-dependency, these effects were not modified by food availability. However, wild juveniles with high SMR had decreased survival when food was scarce, but there was no such effect at high food availability. This study provides further proof that farmed salmon introgression may compromise the viability of wild salmon populations. We cannot, however, conclude that this is connected to alterations in the metabolic phenotype of farmed salmon.

Hydropower impacts on reservoir fish populations are modified by environmental variation.

Global transition towards renewable energy production has increased the demand for new and more flexible hydropower operations. Before management and stakeholders can make informed choices on potential mitigations, it is essential to understand how the hydropower reservoir ecosystems respond to water level regulation (WLR) impacts that are likely modified by the reservoirs' abiotic and biotic characteristics. Yet, most reservoir studies have been case-specific, which hampers large-scale planning, evaluation and mitigation actions across various reservoir ecosystems. Here, we investigated how the effect of the magnitude, frequency and duration of WLR on fish populations varies along environmental gradients. We used biomass, density, size, condition and maturation of brown trout (Salmo trutta L.) in Norwegian hydropower reservoirs as a measure of ecosystem response, and tested for interacting effects of WLR and lake morphometry, climatic conditions and fish community structure. Our results showed that environmental drivers modified the responses of brown trout populations to different WLR patterns. Specifically, brown trout biomass and density increased with WLR magnitude particularly in large and complex-shaped reservoirs, but the positive relationships were only evident in reservoirs with no other fish species. Moreover, increasing WLR frequency was associated with increased brown trout density but decreased condition of individuals within the populations. WLR duration had no significant impacts on brown trout, and the mean weight and maturation length of brown trout showed no significant response to any WLR metrics. Our study demonstrates that local environmental characteristics and the biotic community strongly modify the hydropower-induced WLR impacts on reservoir fishes and ecosystems, and that there are no one-size-fits-all solutions to mitigate environmental impacts. This knowledge is vital for sustainable planning, management and mitigation of hydropower operations that need to meet the increasing worldwide demand for both renewable energy and ecosystem services delivered by freshwaters.

Modelling the effects of stranding on the Atlantic salmon population in the Dale River, Norway.

Rapid dewatering in rivers as a consequence of hydropower operations may cause stranding of juvenile fish and have a negative impact on fish populations. We implemented stranding into an Atlantic salmon population model in order to evaluate long-term effects on the population in the Dale River, Western Norway. Furthermore, we assessed the sensitivity of the stranding model to dewatered area in comparison to biological parameters, and compared different methods for calculating wetted area, the main abiotic input parameter to the population model. Five scenarios were simulated dependent on fish life-stage, season and light level. Our simulation results showed largest negative effect on the population abundance for hydropeaking during winter daylight. Salmon smolt production had highest sensitivity to the stranding mortality of older juvenile fish, suggesting that stranding of fish at these life-stages is likely to have greater population impacts than that of earlier life-stages. Downstream retention effects on the ramping velocity were found to be negligible in the stranding model, but are suggested to be important in the context of mitigation measure design.

Community structure influences species' abundance along environmental gradients.

Species' response to abiotic environmental variation can be influenced by local community structure and interspecific interactions, particularly in restricted habitats such as islands and lakes. In temperate lakes, future increase in water temperature and run-off of terrestrial (allochthonous) dissolved organic carbon (DOC) are predicted to alter community composition and the overall ecosystem productivity. However, little is known about how the present community structure and abiotic environmental variation interact to affect the abundance of native fish populations. We used a space-for-time approach to study how local community structure interact with lake morphometric and climatic characteristics (i.e. temperature and catchment productivity) to affect brown trout (Salmo trutta L.) yield in 283 Norwegian lakes located in different biogeographical regions. Brown trout yield (based on data from standardized survey gill net fishing; g 100 m(-2) gill net night(-1)) was generally lower in lakes where other fish species were present than in lakes with brown trout only. The yield showed an overall negative relationship with increasing temperature and a positive relationship with lake shoreline complexity. Brown trout yield was also negatively correlated with DOC load (measured using Normalized Difference Vegetation Index as a proxy) and lake size and depth (measured using terrain slope as a proxy), but only in lakes where other fish species were present. The observed negative response of brown trout yield to increasing DOC load and proportion of the pelagic open-water area is likely due to restricted (littoral) niche availability and competitive dominance of more pelagic fishes such as Arctic charr (Salvelinus alpinus (L.)). Our study highlights that, through competitive interactions, the local community structure can influence the response of a species' abundance to variation in abiotic conditions. Changes in biomass and niche use of top predators (such as the brown trout), associated with predicted changes in direct and indirect climatic factors, may have further influences on the structure and function of temperate lake ecosystems.

Unimodal response of fish yield to dissolved organic carbon.

Here, we demonstrate a contrasting effect of terrestrial coloured dissolved organic material on the secondary production of boreal nutrient poor lakes. Using fish yield from standardised brown trout gill-net catches as a proxy, we show a unimodal response of lake secondary productivity to dissolved organic carbon (DOC). This suggests a trade-off between positive and negative effects, where the initial increase may hinge upon several factors such as energy subsidising, screening of UV-radiation or P and N load being associated with organic carbon. The subsequent decline in production with further increase in DOC is likely associated with light limitations of primary production. We also show that shallow lakes switch from positive to negative effects at higher carbon loads than deeper lakes. These results underpin the major role of organic carbon for structuring productivity of boreal lake ecosystems.

Direct and indirect climatic drivers of biotic interactions: ice-cover and carbon runoff shaping Arctic char Salvelinus alpinus and brown trout Salmo trutta competitive asymmetries.

One of the major challenges in ecological climate change impact science is to untangle the climatic effects on biological interactions and indirect cascading effects through different ecosystems. Here, we test for direct and indirect climatic drivers on competitive impact of Arctic char (Salvelinus alpinus L.) on brown trout (Salmo trutta L.) along a climate gradient in central Scandinavia, spanning from coastal to high-alpine environments. As a measure of competitive impact, trout food consumption was measured using (137)Cs tracer methodology both during the ice-covered and ice-free periods, and contrasted between lakes with or without char coexistence along the climate gradient. Variation in food consumption between lakes was best described by a linear mixed effect model including a three-way interaction between the presence/absence of Arctic char, season and Secchi depth. The latter is proxy for terrestrial dissolved organic carbon run-off, strongly governed by climatic properties of the catchment. The presence of Arctic char had a negative impact on trout food consumption. However, this effect was stronger during ice-cover and in lakes receiving high carbon load from the catchment, whereas no effect of water temperature was evident. In conclusion, the length of the ice-covered period and the export of allochthonous material from the catchment are likely major, but contrasting, climatic drivers of the competitive interaction between two freshwater lake top predators. While future climatic scenarios predict shorter ice-cover duration, they also predict increased carbon run-off. The present study therefore emphasizes the complexity of cascading ecosystem effects in future effects of climate change on freshwater ecosystems.

Ice-cover effects on competitive interactions between two fish species.

1. Variations in the strength of ecological interactions between seasons have received little attention, despite an increased focus on climate alterations on ecosystems. Particularly, the winter situation is often neglected when studying competitive interactions. In northern temperate freshwaters, winter implies low temperatures and reduced food availability, but also strong reduction in ambient light because of ice and snow cover. Here, we study how brown trout [Salmo trutta (L.)] respond to variations in ice-cover duration and competition with Arctic charr [Salvelinus alpinus (L.)], by linking laboratory-derived physiological performance and field data on variation in abundance among and within natural brown trout populations. 2. Both Arctic charr and brown trout reduced resting metabolic rate under simulated ice-cover (darkness) in the laboratory, compared to no ice (6-h daylight). However, in contrast to brown trout, Arctic charr was able to obtain positive growth rate in darkness and had higher food intake in tank experiments than brown trout. Arctic charr also performed better (lower energy loss) under simulated ice-cover in a semi-natural environment with natural food supply. 3. When comparing brown trout biomass across 190 Norwegian lakes along a climate gradient, longer ice-covered duration decreased the biomass only in lakes where brown trout lived together with Arctic charr. We were not able to detect any effect of ice-cover on brown trout biomass in lakes where brown trout was the only fish species. 4. Similarly, a 25-year time series from a lake with both brown trout and Arctic charr showed that brown trout population growth rate depended on the interaction between ice breakup date and Arctic charr abundance. High charr abundance was correlated with low trout population growth rate only in combination with long winters. 5. In conclusion, the two species differed in performance under ice, and the observed outcome of competition in natural populations was strongly dependent on duration of the ice-covered period. Our study shows that changes in ice phenology may alter species interactions in Northern aquatic systems. Increased knowledge of how adaptations to winter conditions differ among coexisting species is therefore vital for our understanding of ecological impacts of climate change.

Adaptive winter survival strategies: defended energy levels in juvenile Atlantic salmon along a latitudinal gradient.

Current knowledge suggests that patterns of energy storage and depletion in animals are governed by behavioural trade-offs between risks associated with feeding and future energy demands. However, the length of adverse periods varies over geographical or climatic gradients. To explore the potential for genotypic sources of variation in behavioural trade-offs, we compared the winter energy-depletion patterns among 13 wild populations of juvenile Atlantic salmon (Salmo salar L.) along a latitudinal gradient (58-70 degrees N) and performed common-environment experiments of energy-state-dependent feeding. In the wild, winter lipid-depletion rates were lower for northern than for southern populations. The variation in spring lipid levels among the population was lower than autumn variation, with storage lipid levels clustered close to critical limits for survival. In semi-natural stream channels with natural food supply, hatchery-reared fish originating from northern populations showed a positive scaling of feeding activity with decreasing energy levels, whereas southern populations did not. In conclusion, juvenile Atlantic salmon from northern populations defend their energy levels more strongly than fish from southern populations. Adaptive variation in feeding activity appears important for this difference. Thus, the present study shows a link between geographical patterns in storage energy trajectories and adaptive differences in state-dependent feeding motivation.

Spatial distribution of limited resources and local density regulation in juvenile Atlantic salmon.

1. Spatial heterogeneity of resources may influence competition among individuals and thus have a fundamental role in shaping population dynamics and carrying capacity. In the present study, we identify shelter opportunities as a limiting resource for juvenile Atlantic salmon (Salmo salar L.). Experimental and field studies are combined in order to demonstrate how the spatial distribution of shelters may influence population dynamics on both within and among population scales. 2. In closed experimental streams, fish performance scaled negatively with decreasing shelter availability and increasing densities. In contrast, the fish in open stream channels dispersed according to shelter availability and performance of fish remaining in the streams did not depend on initial density or shelters. 3. The field study confirmed that spatial variation in densities of 1-year-old juveniles was governed both by initial recruit density and shelter availability. Strength of density-dependent population regulation, measured as carrying capacity, increased with decreasing number of shelters. 4. Nine rivers were surveyed for spatial variation in shelter availability and increased shelter heterogeneity tended to decrease maximum observed population size (measured using catch statistics of adult salmon as a proxy). 5. Our studies highlight the importance of small-scale within-population spatial structure in population dynamics and demonstrate that not only the absolute amount of limiting resources but also their spatial arrangement can be an important factor influencing population carrying capacity.

Severe mortality in wild Atlantic salmon Salmo salar due to proliferative kidney disease (PKD) caused by Tetracapsuloides bryosalmonae (myxozoa).

Extensive mortality in Atlantic salmon fry was reported in the River Aelva from 2002 to 2004. Dead fish were collected in late summer 2006, and live fish were sampled by electrofishing in September the same year. At autopsy and in histological sections, the fish kidneys were found to be pale and considerably enlarged. Proliferative lesions with characteristic PKX cells were seen in a majority of the fish. DNA from kidney samples of diseased fish was subjected to PCR and sequencing, and the amplified sequences matched those of Tetracapsuloides bryosalmonae. We concluded that this myxozoan transmitted from bryozoans was the main cause of the observed mortality in salmon fry in 2006. Results from quantitative electrofishing in 2005 and 2006, combined with the observed fry mortality from 2002 to 2004, show that the smolt production in the river is severely reduced and that T. bryosalmonae is the most likely explanation for this decline. The present study is the first to report a considerable negative population effect in wild Atlantic salmon due to proliferative kidney disease (PKD). It also represents the northernmost PKD outbreak in wild fish. The river is regulated for hydroelectric power purposes, causing reduced water flow and elevated summer temperatures, and the present PKD outbreak may serve as an example of increased disease vulnerability of northern fish populations in a warmer climate.