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.     

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.     

The feeding behaviour of juvenile Atlantic salmon in relation to turbulent flow

The feeding behaviour of juvenile Atlantic salmon Salmo salar in the Sainte‐Marguerite River, Quebec, Canada, varied with the characteristics of turbulent flow. Simulations indicated that juveniles would decrease their swimming costs during attacks by 19·8% in low and by 31·1% in high turbulent conditions by initiating movements in low‐speed flow events. The real swimming costs did not differ from the swimming costs estimated for a situation where fish initiate their movements at randomly selected flow velocities. The juvenile Atlantic salmon did not seem to prefer low‐speed flow events when initiating their movements. The proportion of time used for movements by fish decreased with an increase in the mean and the s . d . of the flow velocity.     

Artificial light and season affects vertical distribution and swimming behaviour of post-smolt Atlantic salmon in sea cages

In winter, post-smolts of Atlantic salmon Salmo salar exposed to continuous additional light of different intensities (LL) in 14 m deep sea cages maintained a constant swimming speed in circular polarized schools with maximum fish density in the warmest water layers at 11 m depth. By contrast, fish exposed to natural light only (NL) ceased swimming at dusk, ascended from the warm layer to the thermocline c. 3 m depth and were more dispersed in the whole water column during the dark phase. In early spring, fish exposed to LL of medium (LL-MED) or high (LL-HIGH) light intensity ascended and maximum fish density was at 5 m depth. A similar ascent was delayed to late spring in both the low intensity group (LL-LOW) and the NL group, coinciding with a shift in maximum temperature to this depth. The advanced ascent in the LL-HIGH and LL-MED groups is interpreted as a light-induced shift in a seasonal rhythm of feeding motivation. In summer, most of the fish in all four treatment groups were observed in the warm and less saline 4 m surface layer. It is suggested that the seasonal and diel changes in vertical distribution of Atlantic salmon are related inversely to feeding motivation, with preferences for maximum temperature and darkness acting as modifying factors.     

Diet partitioning in sympatric Atlantic salmon and brown trout in streams with contrasting riparian vegetation

Prey intake by Atlantic salmon Salmo salar and brown trout Salmo trutta was measured across different riparian vegetation types: grassland, open canopy deciduous and closed canopy deciduous, in upland streams in County Mayo, Western Ireland. Fishes were collected by electrofishing while invertebrates were sampled from the benthos using a Surber sampler and drifting invertebrates collected in drift traps. Aquatic invertebrates dominated prey numbers in the diets of 0+ year Atlantic salmon and brown trout and 1+ year Atlantic salmon, whereas terrestrial invertebrates were of greater importance for diets of 1+ and 2+ year brown trout. Terrestrial prey biomass was generally greater than aquatic prey for 1+ and 2+ year brown trout across seasons and riparian types. Prey intake was greatest in spring and summer and least in autumn apart from 2+ year brown trout that sustained feeding into autumn. Total prey numbers captured tended to be greater for all age classes in streams with deciduous riparian canopy. Atlantic salmon consumed more aquatic prey and brown trout more terrestrial prey with an ontogenetic increase in prey species richness and diversity. Atlantic salmon and brown trout diets were most similar in summer. Terrestrial invertebrates provided an important energy subsidy particularly for brown trout. In grassland streams, each fish age class was strongly associated with aquatic, mainly benthic invertebrates. In streams with deciduous riparian canopy cover, diet composition partitioned between conspecifics with older brown trout associated with surface drifting terrestrial invertebrates and older Atlantic salmon associated with aquatic invertebrates with a high drift propensity in the water column and 0+ year fish feeding on benthic aquatic invertebrates. Deciduous riparian canopy cover may therefore facilitate vertical partitioning of feeding position within the water column between sympatric Atlantic salmon and brown trout. Implications for riparian management are discussed.     

Behaviour during elevated water temperatures: can physiology explain movement of juvenile Atlantic salmon to cool water?

1. Temperature governs most physiological processes in animals. Ectotherms behaviourally thermoregulate by selecting habitats with temperatures regulating their body temperature for optimal physiological functioning. However, ectotherms can experience temperature extremes forcing the organisms to seek temperature refuge. 2. Fish actively avoid potentially lethal temperatures by moving to cool-water sites created by inflowing tributaries and groundwater seeps. Juvenile Atlantic salmon (Salmo salar) of different age classes exhibit different behavioural responses to elevated temperatures (>23 °C). Yearling (1+) and 2-year-old (2+) Atlantic salmon often cease feeding, abandon territorial behaviour and swim continuously in aggregations in cool-water sites; whereas young-of-the-year (0+) fish continue defending territories and foraging. 3. This study determined whether the behavioural shift in older individuals (2+) occurred when basal metabolic rate, driven by increasing water temperature, reached the maximum metabolic rate such that anaerobic pathways were recruited to provide energy to support vital processes. Behaviour (feeding and stress responses), oxygen consumption, muscle lactate and glycogen, and circulating blood lactate and glucose concentrations were measured in wild 0+ and 2+ Atlantic salmon acclimated to water temperatures between 16 and 28 °C. 4. Results indicate that oxygen consumption of the 2+ fish increased with temperature and reached a plateau at 24 °C, a temperature that corresponded to cessation of feeding and a significant increase in muscle and blood lactate levels. By contrast, oxygen consumption in 0+ fish did not reach a plateau, feeding continued and muscle lactate did not increase, even at the highest temperatures tested (28 °C). 5. To conclude, the experiment demonstrated that the 0+ and 2+ fish had different physiological responses to the elevated water temperatures. The results suggest that wild 2+ Atlantic salmon employ behavioural responses (e.g. movement to cool-water sites) at elevated temperatures in an effort to mitigate physiological imbalances associated with an inability to support basal metabolism through aerobic metabolic processes.     

Thiamin dynamics during the adult life cycle of Atlantic salmon (Salmo salar)

Thiamin is an essential water-soluble B vitamin known for its wide range of metabolic functions and antioxidant properties. Over the past decades, reproductive failures induced by thiamin deficiency have been observed in several salmonid species worldwide, but it is unclear why this micronutrient deficiency arises. Few studies have compared thiamin concentrations in systems of salmonid populations with or without documented thiamin deficiency. Moreover, it is not well known whether and how thiamin concentration changes during the marine feeding phase and the spawning migration. Therefore, samples of Atlantic salmon (Salmo salar) were collected when actively feeding in the open Baltic Sea, after the sea migration to natal rivers, after river migration, and during the spawning period. To compare populations of Baltic salmon with systems without documented thiamin deficiency, a population of landlocked salmon located in Lake Vänern (Sweden) was sampled as well as salmon from Norwegian rivers draining into the North Atlantic Ocean. Results showed the highest mean thiamin concentrations in Lake Vänern salmon, followed by North Atlantic, and the lowest in Baltic populations. Therefore, salmon in the Baltic Sea seem to be consistently more constrained by thiamin than those in other systems. Condition factor and body length had little to no effect on thiamin concentrations in all systems, suggesting that there is no relation between the body condition of salmon and thiamin deficiency. In our large spatiotemporal comparison of salmon populations, thiamin concentrations declined toward spawning in all studied systems, suggesting that the reduction in thiamin concentration arises as a natural consequence of starvation rather than to be related to thiamin deficiency in the system. These results suggest that factors affecting accumulation during the marine feeding phase are key for understanding the thiamin deficiency in salmonids.     

The relationship between otolith accretion and resting metabolic rate in juvenile Atlantic salmon during a change in temperature

This study confirmed earlier evidence for a correlation between otolith increment width and resting metabolic rate in the absence of somatic growth in Atlantic salmon parr. However, increment width responded more conservatively to a change in temperature than did resting metabolic rate. Consequently, the study demonstrated that although increment width varied with temperature the process governing accretion rate was not simply related to resting metabolic rate.     

Is there a threshold size regulating seaward migration of brown trout and Atlantic salmon?

We investigated the influence of variation in body size and growth rate on age of smolting in Atlantic salmon and brown trout in four different Norwegian rivers. In Atlantic salmon smolt ages varied between 2 and 6 years, and in brown trout between 2 and 7 years. Smolt age was negatively correlated with parr growth, and positively correlated with smolt size. Age at smolting was more variable in the two northern than the two southern rivers. Smolt sizes and ages were also more variable in brown trout than in Atlantic salmon. Based on the observed variation in smolt size and age, we reject the hypothesis that a threshold size alone regulates age at smolting. Within populations smolt age depends on growth rate so that fast-growing parr smolted younger and smaller than slow-growing parr. We hypothesize that smolt size and age is a trade-off between expected benefits and costs imposed by differences in individual growth rate.     

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.     

The relationships between specific dynamic action,nutrient retention and feed conversion ratio in farmed freshwater Chinook salmon (Oncorhynchus tshawytscha)

Improving the feed conversion ratio (FCR; the amount of feed consumed relative to the amount of weight gain) can reduce both production costs and environmental impacts of farmed fish. The aim of this study was to investigate what drives FCR to understand how nutrients are retained, as well as the amount of oxygen consumed for digestion, absorption and assimilation (a metabolic process known as specific dynamic action, SDA). Feed-efficient and inefficient Chinook salmon (Oncorhynchus tshawytscha) in fresh water were identified using ballotini beads and X-radiography that tracked individual feed intake across three assessment periods under satiated feeding. This allowed a comparison of physiological traits and body composition between the two FCR phenotypes over two time points as Chinook salmon grew from 305 to 620 g. Fish with higher daily feed intake (DFI) had higher daily weight gain (DWG) as expected. Nonetheless, the relationship between FCR and DFI as well as FCR and DWG was variable between time points. FCR and DWG were not correlated at the first time point and were negatively correlated at the second time point. In contrast, FCR and DFI were positively correlated at the first time point but not the second. Despite this, efficient fish ate smaller meals and retained more protein, lipid and energy in their body tissues. There was no detectable difference in metabolism between the two FCR phenotypes with respect to minimal resting metabolic rate, maximum metabolic rate, aerobic scope, or SDA parameters. In conclusion, FCR is not consistently associated with growth and metabolic differences in freshwater Chinook salmon, but FCR-efficient fish retain more nutrients and consume smaller meals.     

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.     

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°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.     

Apparent digestibility coefficients and accumulation of astaxanthin E/Z isomers in Atlantic salmon (Salmo salar L.) and Atlantic halibut (Hippoglossus hippoglossus L.)

Apparent astaxanthin (3,3'-dihydroxy-beta,beta-carotene-4,4'-dione) digestibility coefficients (ADC) and carotenoid compositions of the muscle, liver, whole kidney and plasma were compared in Atlantic salmon (Salmo salar) and Atlantic halibut (Hippoglossus hippoglossus) fed a diet supplemented with 66 mg astaxanthin kg(-1) dry matter for 112 days. The astaxanthin source consisted of 75% all-E-, 3% 9Z- and 22% 13Z-astaxanthin, of (3R,3'R)-, (3R,3'S; meso)-, and (3S,3'S)-astaxanthin in a 1:2:1 ratio. The ADC of astaxanthin was significantly higher in Atlantic halibut than in Atlantic salmon after 56 and 112 days of feeding (P < 0.05). The ADC of all-E-astaxanthin was significantly higher than ADC of 9Z-astaxanthin (P < 0.05). Considerably more carotenoids were present in all plasma and tissue samples of salmon than in halibut. Retention of astaxanthin in salmon muscle was 3.9% in salmon and 0 in halibut. All-E-astaxanthin accumulated selectively in the muscle of salmon, and in plasma of salmon and halibut compared with diet. 13Z-astaxanthin accumulated selectively in liver and whole kidney of salmon and halibut, when compared with plasma. A reductive pathway for astaxanthin metabolism in halibut similar to that of salmon was shown by the presence of 3',4'-cis and trans glycolic isomers of idoxanthin (3,3',4'-trihydroxy-beta,beta-carotene-4'-one) in plasma, liver and whole kidney. In conclusion, the higher ADC of astaxanthin in halibut than Atlantic salmon may be explained by lower feed intake in halibut, and the lower retention of astaxanthin by a higher capacity to transform astaxanthin metabolically.     

Phenotypic flexibility and physiological tradeoffs in the feeding and growth of marine bivalve molluscs

Bivalve molluscs have a highly plastic feeding and growth physiology.The increasing availability of families artificially selectedfor faster growth has enabled physiological experiments to investigatethe genetic basis for variable rates of growth. Fast growthis achieved by a combination of increased rates of feeding,reduced metabolic rates and lower metabolic costs of growth.In at least one species there is a trade-off between growthin protein and the storage of lipids that are utilized in gametogenesis.Energy requirements for maintenance are also higher in slow-growingindividuals. Reduced costs of growth are due in part to increasedefficiencies of protein turnover. Nevertheless, high proteinturnover (and therefore high metabolic cost) may benefit fitnessin the later stages of gametogenesis. Faster feeding rates donot impair flexibility in feeding behavior which compensatesfor changes in the food environment. Both inter- and intra-speciesdifferences in feeding behavior are evident and suggest possibleconstraints imposed by faster feeding on the efficiency of selectionbetween food particles of different nutritional value.     

Underyearling pink and chum salmon in the western Bering Sea during the fall season (September and October 2013): Distribution,feeding habits,and growth patterns

The ontogeny of a year class of pink and chum salmon is described for the period after the redistribution of underyearling individuals from coastal waters to deep-sea areas of the western Bering Sea in September and October, 2013. The intensity of their feeding was high; their diet included hyperiids, pteropods, and juvenile euphausiids. The metabolic costs of growth reached only 20% of the consumed food, which indicates significant energy costs for locomotion; moreover, as the body size increases, the level of metabolic functions rises at a decreasing rate, which causes the body growth to slow down and food consumption to decrease. The main items in the diet of underyearling salmon are characterized by a low content of dry matter, low lipid content, and, consequently, a low calorie content, i.e., underyearlings mainly consume protein-rich food with a low fat content. The chemical composition of the tissues almost did not differ between underyearling pink and chum salmon. Both species typically had a low fat content in their muscles. Thus, fat is not accumulated at this stage of ontogeny; all energy that is obtained with food, after being used for locomotion and metabolism, is spent for linear growth.     

The survival of semi‐wild, wild and hatchery‐reared Atlantic salmon smolts of the Simojoki River in the Baltic Sea

The recapture rate and survival of hatchery‐reared Atlantic salmon Salmo salar stocked as 1 year‐old parr (semi‐wild) with that of hatchery‐reared Atlantic salmon stocked as 2 year‐old smolts and wild smolts of Atlantic salmon in the northern Baltic Sea were compared. This was done through tagging experiments carried out in 1986–1988 and 1992. The recapture rate of the semi‐wild groups varied from 1·0 to 13·1%, being similar in 3 tagging years and lower in 1 year than that of the wild groups (1·7–17·0%). The recapture rate of the semi‐wild groups was similar (in 2 years) or higher (in 2 years) than that of the hatchery‐reared groups stocked as smolts (1·3–6·3%). The survival of semi‐wild smolts during the sea migration was as high as that of wild Atlantic salmon of an equal size and two to three times higher than hatchery‐reared Atlantic salmon stocked as smolts. The survival rate was positively associated with smolt size. The suitability of hatchery‐reared parr and smolts in the management of reduced Atlantic salmon stocks is compared.     

Atlantic salmon straying from the River Imsa

Mean estimated straying rate for Atlantic salmon Salmo salar L. leaving the River Imsa as smolts during 1976–1999 was 15% for hatchery fish and 6% for wild conspecifics. Hatchery Atlantic salmon selected for production traits during four or more generations strayed >50%. The straying rate was higher for Atlantic salmon staying 2 rather than 1 year at sea before attaining maturity. For spawning, 96% of the strays entered streams within 420 km from the River Imsa, and c . 80% entered streams within 60 km of the mouth of the River Imsa, whether the fish were wild or hatchery released. Within the 60 km zone, the number of strays caught in a river increased with the Atlantic salmon catch in that river, but there was no significant relationship between straying rate and water discharge or distance from the river to the River Imsa. The observed straying rate of hatchery Atlantic salmon decreased with increasing number of fish entering the River Imsa. Sexual maturation as parr did not influence the tendency to stray. The results suggest that the establishment of temporary zones, free of fish farms, outside important Atlantic salmon rivers by the fisheries authorities in Norway should be large, whole fjords, to be effective.     

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.     

Increasing temperature associated with increasing grilse proportion and smaller grilse size of Atlantic salmon

Effects of temperature on Atlantic salmon (Salmo salar) were analysed using Carlin tag recovery data (1985–2014), and mixed-stock catch data (smolt years from 2001 to 2012) in northern parts of the Baltic Sea. During warmer summers, the mean smolt length of the recaptured salmon tended to be smaller, and salmon were recaptured more frequently in feeding grounds closer to the home rivers in the Gulf of Bothnia, while colder summers were associated with more recaptures further south, in the Baltic Main Basin. Moreover, a warmer spring in the smolt year was associated with decreased weight of male grilses in mixed stock data. Further, warmer spring temperatures during the smolt year were associated with a higher proportion of one-sea-winter (1SW) males during the return migration in mixed stock data. These results suggest that the increasing global temperature may affect Atlantic salmon life history demographics.