The stability of standard metabolic rate during a period of food deprivation in juvenile Atlantic salmon

Among juvenile Atlantic salmon Salmo salar either being fed ad libitum throughout a 3 month experiment or deprived of food in the middle month, food deprivation led to a decrease in SMR, which increased again once food was supplied ad libitum again. While the rank order of SMR among fish fed throughout remained relatively stable, that within the deprived group was inconsistent, suggesting that individual fish vary in their ability to reduce metabolic costs when food availability is low.     

Effects of food ration on SMR: influence of food consumption on individual variation in metabolic rate in juvenile coho salmon (Onchorhynchus kisutch)

1. Consistency of differences in standard metabolic rate (SMR) between individual juvenile salmonids and the apparently limited ability of individuals to regulate their SMR has led many researchers to conclude that differences in individual SMR are fixed (i.e. genetic). 2. To test for the effects of food ration on individual performance and metabolism, SMR was estimated by measuring oxygen consumption using flow-through respirometry on individually separated young of the year coho salmon (Oncorhynchus kisutch) placed on varying food rations over a period of 44 days. 3. Results demonstrate that the quantity of food consumed directly affects SMR of juvenile coho salmon, independent of specific dynamic action (SDA, an elevation in metabolic rate from the increased energy demands associated with digestion immediately following a meal) and indicates that higher food consumption is a cause of elevated SMR rather than a consequence of it. Juvenile coho salmon therefore demonstrated an ability to regulate their SMR according to food availability and ultimately food consumption. 4. This study indicates that food consumption may play a pivotal role in understanding individual variation in SMR independent of inherent genetic differences. We suggest that studies involving SMR need to be cautious about the effects of intra-individual differences in food consumption in communal tanks or in different microhabitats in the wild as disproportionate food consumption may contribute more to variation in SMR than intrinsic (genetic) factors. 5. In general, our results suggest that evolutionary changes in SMR are likely a response to selection on food consumption and growth, rather than SMR itself.     

Temporal repeatability of relative standard metabolic rate in juvenile Atlantic salmon and its relation to life history variation

There was a strong correlation between the relative standard metabolic rate (rSMR) values of individual Atlantic salmon Salmo salar L. measured 5 and 22 weeks after first feeding in June and October respectively (Pearson's r =0·68, 26 d.f., P <0·001). However, this is a conservative estimate of repeatability as two separate regressions were used to calculate SMR in October due to the separation of the population into an upper modal group made up of early migrants and a lower modal group comprised of delayed migrants. SMR values in June and October were similar (paired t test, t =-0·85, 27 d.f., P >0·05) when expressed as the percentage deviation from those predicted for a fish of that size based on the body mass/SMR relations in June or October indicating that relative standard metabolic rates were stable over time when food was not limiting. rSMR status was maintained in 19 of the 28 fish (i.e. 68%) between the two measures. rSMR status was correlated with life history strategy: salmon fry with a high SMR in June were more likely to become smolts during the autumn than those with a low SMR.     

Adaptive trade-offs in juvenile salmonid metabolism associated with habitat partitioning between coho salmon and steelhead trout in coastal streams

1. Adaptive trade-offs are fundamental to the evolution of diversity and the coexistence of similar taxa and occur when complimentary combinations of traits maximize efficiency of resource exploitation or survival at different points on environmental gradients. 2. Standard metabolic rate (SMR) is a key physiological trait that reflects adaptations to baseline metabolic performance, whereas active metabolism reflects adaptations to variable metabolic output associated with performance related to foraging, predator avoidance, aggressive interactions or migratory movements. Benefits of high SMR and active metabolism may change along a resource (productivity) gradient, indicating that a trade-off exists among active metabolism, resting metabolism and energy intake. 3. We measured and compared SMR, maximal metabolic rate (MMR), aerobic scope (AS), swim performance (UCrit) and growth of juvenile hatchery and wild steelhead and coho salmon held on high- and low-food rations in order to better understand the potential significance of variation in SMR to growth, differentiation between species, and patterns of habitat use along a productivity gradient. 4. We found that differences in SMR, MMR, AS, swim performance and growth rate between steelhead trout and coho salmon were reduced in hatchery-reared fish compared with wild fish. Wild steelhead had a higher MMR, AS, swim performance and growth rate than wild coho, but adaptations between species do not appear to involve differences in SMR or to trade-off increased growth rate against lower swim performance, as commonly observed for high-growth strains. Instead, we hypothesize that wild steelhead may be trading off higher growth rate for lower food consumption efficiency, similar to strategies adopted by anadromous vs. resident brook trout and Atlantic salmon vs. brook trout. This highlights potential differences in food consumption and digestion strategies as cryptic adaptations ecologically differentiating salmonid species. 5. We hypothesize that divergent digestive strategies, which are common and well documented among terrestrial vertebrates, may be an important but overlooked aspect of adaptive strategies of juvenile salmonids, and fish in general.     

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.     

Functional models for growth and food consumption of Atlantic salmon parr, Salmo salar, from a Norwegian river

1. The chief objectives were to analyse and model experimental data for maximum growth and food consumption of Atlantic salmon parr (Salmo salar) collected from a cold glacier fed river in western Norway. The growth and feeding models were also applied to groups of Atlantic salmon growing and feeding at rates below the maximum. The growth models were validated by comparing their predictions with observed growth in the river supplying the experimental fish.
2. Two different models were fitted, one originally developed for British salmon and the other based on a model for bacterial growth. Both gave estimates for optimum temperature for growth at 18–19 °C, somewhat higher than for Atlantic salmon from Britain. Higher optimal temperature for growth in salmon from a cold Norwegian river than from British rivers does not concur with predictions from the thermal adaptation hypothesis.
3. Model parameter estimates differed among growth groups in that the lower critical temperature for growth increased from fast to slow growing individuals. In contrast to findings for brown trout (Salmo trutta), the optimum temperature for growth did not decrease with decreasing levels of food consumption.
4. A new and simple model showed that food consumption (expressed in energy terms) peaked at 19.5–19.8 °C, which is similar to the optimal temperature for growth. Feeding began at a temperature 1.5 °C below the lower temperature for growth and ended about 1 °C above the maximum temperature for growth. Model parameter estimates for consumption differed among growth groups in a manner similar to the growth models. Maximum consumption was lower for Atlantic salmon than for brown trout, except at temperatures above 18 °C.
5. By combining the growth and food consumption models, growth efficiency was estimated and reached a maximum at about 14 °C for fast growing individuals, increasing to nearly 17 °C for slow growing ones, although it was lower overall for the latter group. Efficiency also declined with increasing fish size. Growth efficiency was generally higher for Atlantic salmon than for brown trout, particularly at high temperature.     

Growth depensation and aggression in laboratory reared coho salmon: the effect of food distribution and ration size

Groups of recently emerged coho salmon fry Oncorhynchus kisutch were reared for 3 months on food that appeared either asynchronously at a single location (localized) or synchronously and spatially dispersed (dispersed). Groups were further subdivided into those receiving low (1%) or high (3% body weight per day) rations, with five replicate groups for each treatment combination. At low ration there was greater growth depensation, i.e. growth variation, in groups receiving localized as compared to dispersed food. At high ration there was no difference. There was no effect of food distribution upon mean fish weight, but groups receiving high rations had greater mean fish weights than groups receiving low rations. There was no overall difference in the frequency of chasing between any of the treatment combinations. However, in localized food groups, dominants defended positions close to where food entered the tank, giving them greater access than subordinates. In dispersed food groups, while dominants also defended particular areas, this did not result in greater access to food. These results demonstrate that although feeding methodology may not directly influence the frequency of aggressive interactions, feeding methods which facilitate food monopolization by dominants can accelerate the growth of these individuals at the expense of subordinates. In aquacultural applications where greater size is desirable, or otherwise selected for, this may result in the unintentional selection for increased aggressiveness.     

Effects of body size on sympatric shelter use in over‐wintering juvenile salmonids

The study tests two hypotheses: (1) the degree of shelter dominance in Atlantic salmon Salmo salar and brown trout Salmo trutta increases progressively with increasing size differential between heterospecific fish in a pair and (2) shelter dominance, standardized to size differential, correlates with aggression. The results support the first but not the second hypothesis, suggesting that the fitness consequences of high growth performance during the summer are likely to become evident during winter. At this time of year, when mortality is high among both Atlantic salmon and brown trout, shelter dominance may increase the chances of survival.     

Competition between brown trout and Atlantic salmon parr over pool refuges during rapid dewatering

Variations in distributions and behaviours of Atlantic salmon Salmo salar in allopatry (homogeneous) and in sympatry with brown trout Salmo trutta (mixed) were observed before, during and after 2 day periods of dewatering in a large glass-sided indoor stream at densities typical of Scottish upland streams. Brown trout utilized pools more than Atlantic salmon at normal flows and in both species the majority of fishes moved into pools during dewatering. There was no significant effect of brown trout, which was the more dominant species, on the overall ability of Atlantic salmon to use pool habitat as a refuge during dewatering. Within mixed and homogeneous groups, average feeding levels decreased during dewatering. The highest ranking fish, which was always a brown trout in mixed groups, predominantly monopolized the pool and other individuals in pools adopted a more cryptic, stationary behaviour. Dewatering effectively increased local population density with the result that dominance status became much more important in maintaining food intake, and polarization between the top ranking fish and others increased. During the first day of dewatering, there was extreme behavioural polarization such that the dominant fish exhibited most aggression and least feeding within the group. Among dominant fish on the second day of dewatering, aggression had largely abated and feeding had returned to pretreatment levels despite the reduced average feeding within the group. The main difference between mixed and homogeneous groups was in the behaviour of the most dominant Atlantic salmon, which was near-despotic in allopatry and subordinate to brown trout in sympatry.     

The performance advantage of a high resting metabolic rate in juvenile salmon is habitat dependent

1.?Basal levels of metabolism vary significantly among individuals in many taxa, but the effects of this on fitness are generally unknown. Resting metabolic rate (RMR) in juvenile salmon and trout is positively related to dominance status and ability to obtain a feeding territory, but it is not clear how this translates into performance in natural conditions. 2.?The relationships between RMR, dominance, territoriality and growth rates of yearling Atlantic salmon Salmo salar were examined in relation to predictability in food supply and habitat complexity, using replicate sections of a large-scale controlled semi-natural stream. 3.?Estimated RMR was a strong predictor of dominance, and under conditions of a predictable food supply in a structurally simple habitat, high estimated RMR fish obtained the best feeding territories and grew faster. 4.?When the spatial distribution of food was made less predictable, dominant (high estimated RMR) fish were still able to occupy the most profitable feeding locations by periodically moving location to track the changes in food availability, but RMR was no longer a predictor of growth rate. Moreover, when a less predictable food supply was combined with a visually more complex (and realistic) habitat, fish were unable to track changes in food availability, grew more slowly and exhibited greater site fidelity, and there were no relationships between estimated RMR and quality of occupied territory or growth rate. 5.?The relative benefit of RMR is thus context dependent, depending on both habitat complexity and the predictability of the food supply. Higher habitat complexity and lower food predictability decrease the performance advantages associated with a high RMR.     

Juvenile salmon with high standard metabolic rates have higher energy costs but can process meals faster

Basal or standard metabolic rate (SMR) has been found to exhibit substantial intraspecific variation in a range of taxa, but the consequences of this variation are little understood. Here we explore how SMR is related to the energy cost of processing food, known as apparent specific dynamic action or the heat increment of feeding. Using juvenile Atlantic salmon Salmo salar, we show that fishes with a higher SMR had a higher peak and a greater total energy expenditure when digesting a given size of meal. However, the duration over which their metabolism was elevated after consuming the meal was shorter. The greater energy costs they incur for processing food may be related to their assimilation efficiency. These relationships are likely to have implications for feeding strategies and growth rates, since individuals with a higher SMR have higher routine costs of living but recover more quickly following feeding and so may have a greater potential for processing food.     

Do Low-Mercury Terrestrial Resources Subsidize Low-Mercury Growth of Stream Fish? Differences between Species along a Productivity Gradient

Low productivity in aquatic ecosystems is associated with reduced individual growth of fish and increased concentrations of methylmercury (MeHg) in fish and their prey. However, many stream-dwelling fish species can use terrestrially-derived food resources, potentially subsidizing growth at low-productivity sites, and, because terrestrial resources have lower MeHg concentrations than aquatic resources, preventing an increase in diet-borne MeHg accumulation. We used a large-scale field study to evaluate relationships among terrestrial subsidy use, growth, and MeHg concentrations in two stream-dwelling fish species across an in-stream productivity gradient. We sampled young-of-the-year brook trout (Salvelinus fontinalis) and Atlantic salmon (Salmo salar), potential competitors with similar foraging habits, from 20 study sites in streams in New Hampshire and Massachusetts that encompassed a wide range of aquatic prey biomass. Stable isotope analysis showed that brook trout used more terrestrial resources than Atlantic salmon. Over their first growing season, Atlantic salmon tended to grow larger than brook trout at sites with high aquatic prey biomass, but brook grew two-fold larger than Atlantic salmon at sites with low aquatic prey biomass. The MeHg concentrations of brook trout and Atlantic salmon were similar at sites with high aquatic prey biomass and the MeHg concentrations of both species increased at sites with low prey biomass and high MeHg in aquatic prey. However, brook trout had three-fold lower MeHg concentrations than Atlantic salmon at low-productivity, high-MeHg sites. These results suggest that differential use of terrestrial resource subsidies reversed the growth asymmetry between potential competitors across a productivity gradient and, for one species, moderated the effect of low in-stream productivity on MeHg accumulation.     

Development of spinal deformities in Atlantic salmon and Arctic charr fed diets supplemented with oxytetracycline

Some individuals within populations of Atlantic salmon Salmo salar and Arctic charr Salvelinus alpinus fed diets supplemented with oxytetracycline (OTC) developed spinal deformations. Possible differences in feed intake and growth of spinally deformed fish relative to fish without any deformities were investigated. Amongst Atlantic salmon, 17% of the fish fed OTC-supplemented feed developed spinal fractures, whereas none of the fish receiving the basic feed did so. Despite deformation of the spinal column, the injured fish continued to feed and grow, but at lower rates than unaffected individuals. In contrast to Atlantic salmon, Arctic charr showed no signs of spinal fractures at any time during the 65-day experiment.     

Social status and growth rates as determinants of site attachment in juvenile Atlantic salmon

This paper describes an experimental study of the effects of food supply, growth rates and social interactions on homing by juvenile Atlantic salmon Salmo salar in response to displacement. Groups of five fish were housed in a section of an artificial stream and given either rations allowing maximum growth (the rich condition) or 0·1 of this amount (the poor condition); daily specific growth rates were significantly higher in the rich condition. After a 6-day settlement period, the fish were captured, displaced downstream and their movements recorded over the next 3 h. Prior to displacement, the fish showed a high degree of site fidelity and high levels of aggression. Dominant fish and those with stronger site attachment grew faster prior to displacement, these effects being independent. Following displacement, 24% of all fish returned to their previously favoured site and stayed there, 23% returned home initially, but subsequently moved on, 5% settled in a new site and 49% failed to move. The distribution of responses was identical for the rich and poor conditions, but fish that homed were dominant and had grown faster during the pre-displacement period.     

Allozyme heterozygosity, date of first feeding and life history strategy in Atlantic salmon

The relations between allozyme heterozygosity, relative date of first feeding and life history strategy in juvenile Atlantic salmon Salmo salar were examined using eggs obtained from a 400 family cross (20 male × 20 female adult Atlantic salmon). Multilocus heterozygosity, through its positive associations with the timing of first feeding and growth rate, was correlated with life history strategy in juvenile Atlantic salmon, albeit under genotype × environmental (temperature, food availability) regulation. Under hatchery conditions, a 10 day difference was observed in the relative date of first feeding between early and late first feeding Atlantic salmon. Early first feeding Atlantic salmon exhibited a significantly higher mean heterozygosity, grew faster at ambient water temperature (April to November) and a significantly higher proportion adopted the early freshwater maturation (age 0+ years, male fish) or early migrant (age 1+ years, mainly female fish) strategies compared to late first feeding Atlantic salmon. Elevated water temperatures over the winter (December to April, >10·5° C) provided additional growth opportunity allowing previously mature male parr (mainly early first feeders) and lower modal group parr (mainly late first feeders) to adopt the early migrant strategy by the following spring.     

Juvenile Atlantic salmon in the Varzuga River (White Sea Basin)

In the Varzuga River (Kola Peninsula), juvenile Atlantic salmon occur at a high mean density of 1·1 individuals per m², with a relatively low growth rate, reaching c. 8 g at age 3. They migrate to sea at ages 2–4 before they are fully silvered. Mortality is not high and the fish forage in the estuary where they grow fast and acclimate to the pelagic and high salinity habitat.     

Effects of discharge and local density on the growth of juvenile Atlantic salmon Salmo salar

The study explored the combined effects of density, physical habitat and different discharge levels on the growth of juvenile Atlantic salmon Salmo salar in artificial streams, by manipulating flow during both summer and winter conditions. Growth was high during all four summer trials and increased linearly with discharge and mean velocity. Differences in fish densities (fish m^?3) due to differences in stream volume explained a similar proportion of the variation in mean growth among discharge treatments. Within streams, the fish aggregated in areas of larger sediment size, where shelters were probably abundant, while growth decreased with increasing densities. Fish appeared to favour the availability of shelter over maximization of growth. Mean growth was negative during all winter trials and did not vary among discharge treatments. These results suggest that increased fish densities are a major cause of reduced summer growth at low discharge, and that habitat‐mediated density differences explain the majority of the growth variation across habitat conditions both during summer and winter.     

The influence of food distribution upon the development of aggressive and competitive behaviour in juvenile chum salmon, Oncorhynchus keta

Groups of juvenile chum salmon were reared on food that was either dispersed throughout, or localized in one area of, the rearing tank. Groups receiving localized food displayed more aggression than those receiving dispersed food. This led to differences in growth, with fish reared on localized food having greater individual growth variability, i.e. growth depensation. However, after several months of rearing in these different feeding/social environments, fish reared on dispersed food were just as aggressive when first exposed to localized food as were fish reared on localized food. Furthermore, in competitive contests between fish of the two rearing histories, those reared on dispersed food were just as likely to become dominant as those reared on localized food. These results suggest that the behavioural development of aggressiveness is not amenable to alteration by manipulation of food distribution.     

Effects of size asymmetry on aggression and food acquisition in Arctic charr

The feeding rate of a group (DS) of two small, two medium and two large 1+ Arctic charr Salvelinus alpinus was higher than in a group of six fish of the same size (SS), suggesting that size distribution had an effect on feeding behaviour, with a correlation between the size of the fish and the amount of food eaten–the largest fish eating the most. Against predictions, rate of aggression was not higher in the SS groups; rather there was a modest tendency of higher aggression among individuals in the DS groups.     

Determination of body shape variation in Irish hatchery‐reared and wild Atlantic salmon

Discriminant function analysis was used to distinguish morphologically between samples of parr, smolts and adult Atlantic salmon Salmo salar from several hatchery and river systems in Ireland. The effect of habitat shift was investigated in Atlantic salmon parr. Parr grown from the eyed‐egg stage with a non‐sibling group in a hatchery environment, came to resemble the mean body shape of their host hatchery Atlantic salmon stock more closely than that of a full sibling group grown at their natal hatchery. Wild Atlantic salmon smolts differed in shape from hatchery‐reared smolts. This difference was less pronounced, but still statistically significant when wild adults were compared with hatchery‐reared adults captured in the coastal drift‐net fishery after a year spent at sea. Rearing conditions had a significant impact on the production and growth of fish body shape. This in turn may have affected adaptability and survivorship of ranched Atlantic salmon in the marine environment.