4 The Physiology of Smolting Salmonids

doi:10.1016/S1546-5098(08)60216-2

Fish Physiology

Volume 11, Part B, 1988, Pages 275-343

https://doi.org/10.1016/S1546-5098(08)60216-2 Get rights and content

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This chapter describes the different aspects of the physiology of smolting salmonids. Many salmonids—the fish of the genera, Oncorhynchus, Salmo, and Salvelinus—are anadromous and undergo a distinct transformation prior to seaward migration. Several morphological and physiological changes occur during smolting. Silvering is because of the synthesis of two purines–guanine and hypoxanthine. The needle-like crystals of these substances are deposited in two distinct skin layers: one directly beneath the scales and the other deep in the dermis adjacent to the muscles. The salmonids, as many other temperate-zone animals, have a seasonally changing physiology that is manifested in the cycles of growth, precisely timed migrations, and the seasons of reproduction geared to the most favorable seasons for the birth and development of the young. There is a circannual rhythm of physiological changes associated with the parr–smolt transformation. After juvenile salmon reach a certain critical size, they become smolts with a capacity to hypoosmoregulate and grow in seawater and behavioral changes result in a downstream migration.

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Cited by (774)

Metabolomic responses of Atlantic salmon (Salmo salar) cultured during the pre-smolt, smolt and post-smolt stages
2024, Aquaculture
Atlantic salmon (Salmo salar) is an anadromous salmonid that commonly undergoes a transfer from land-based freshwater hatcheries to ocean-based sea pens for cultivation. For investigating the metabolomic response properties in the cultured Atlantic salmon (∼ 400 g, n = 8 in each group) during the pre-smolt, smolt and post-smolt stages, we performed LC-MS/MS metabolomics to assess the metabolomic responses on the brain and skin of Atlantic salmon. A total of 153 and 115 differentially expressed metabolites (DEMs) exhibited significant variations in the brain and skin, respectively. These metabolites were mainly involved in three metabolic categories of amino acids, organic acids and fatty acids. In the brain, metabolites associated with cortisol synthesis and secretion and biosynthesis of cofactors were highly induced in the smolt stage compared to the pre-smolt stage, while in the post-smolt stage, levels of lipid and amino acid notably reduced. Moreover, 3-(3-hydroxyphenyl) propanoic acid, mannose 6-phosphate, cortisol, thymine, and guanine, as candidate smolting metabolites in the brain, displayed life stage-dependent alterations. In the skin, 3-methoxytyramine, L-sepiapterin, and nucleotide metabolism differed significantly during smoltification. Overall, these results reveal diverse life-stage-associated metabolomic responses in Atlantic salmon and provide important information for the aquaculture of Atlantic salmon.
Genome-wide identification and quantification of salinity-responsive Na<sup>+</sup>/K<sup>+</sup>-ATPase α-subunits in three salmonids
2024, Aquaculture
Na⁺/K⁺-ATPase (NKA) is a ubiquitous ion-transporting pump that functions to maintain intracellular homeostasis. We performed a comprehensive assessment of salinity response in terms of genome-wide identification, evolutionary footprint, structural characterization, expression patterns of NKA α-subunit genes and NKA activity in three salmonids, including rainbow trout (Oncorhynchus mykiss), steelhead trout (O. mykiss irideus), and Atlantic salmon (Salmo salar). From the O. mykiss and S. salar genomes, a total of 48 NKAα genes were identified and classified into nine isoforms: NKAα1 (a/b/b2/c), NKAα2 (a/b), and NKAα3 (a/b/b2). The intergenomic homologous genes across O. mykiss and S. salar exhibited multicollinearity relationships, with two tandem duplicate events occurring mainly in NKAα1b/b2 and α1c. The predicted motifs and domains of NKAα genes were highly conserved, accompanied by unequal transmembrane domains (TMDs) that contained specific functional sites (Na⁺-K⁺/ATP/phosphorylation). The expression profiles of the nine NKAα isoforms in three salmonids were tissue-specific, and the expression levels of NKAα1 except α1c were the highest in the osmoregulatory organs (e.g. gill and mesonephros), while those of NKAα2/α3 were mainly in the excitable tissues (e.g. muscle and brain). Exploration of potential indicators for three salmonids as follows: In the rainbow trout, NKAα2a and NKAα1b/b2 expression were extremely sensitive to salinity change in the gill following transfer to seawater. In the steelhead trout, NKAα3 (a/b/b2) responded more significantly in the heart. In the Atlantic salmon, NKAα1b/b2 isoforms were more prominent in the muscle exposed to seawater. These changes in expression of NKAα were associated with increased NKA activity in the gill and muscle and exhibited salinity-dependent variation and differences between the osmoregulatory capacity of parr and smolt. These results provide insights into the molecular mechanisms of NKAα-mediated salinity sensitivity as well as deliver effective indicators for elucidating the osmoregulation strategy of salmonids.
Salinity induced changes in the progression of water, ion and nutrient fluxes along the gastrointestinal tract of Atlantic salmon smolt (Salmo salar)
2024, Aquaculture
Water ingestion in fish increases with both water salinity and feeding. However, it is unclear whether, during feeding, water ingestion is intended to aid chyme liquefaction in the stomach or to maintain the osmotic homeostasis within the body of the fish. We investigated the effects of increasing water salinity (0, 10, 20, 35 ppt) on the progression of water, ion and nutrient fluxes in the gastrointestinal tract of Atlantic salmon smolt (Salmo salar) fed a commercial-like diet. Furthermore, the effect of water salinity on blood pH, plasma osmolality and ions was investigated. The experiment lasted for 8 weeks. Chyme was collected from 4 gastrointestinal tract (GIT) segments (stomach, proximal, middle and distal intestine) and analysed for dry matter, pH, osmolality, crude protein and mineral content. Water and electrolyte fluxes, kinetic of digestion and faecal digestibility were measured using yttrium oxide (Y₂O₃) as an inert marker. We found that between 0 and 35 ppt chyme dry matter decreased by 1.6% and 4.8% in the stomach and proximal intestine, respectively. Chyme pH was not affected by water salinity in the stomach, but it increased linearly (p < 0.001) with salinity in all intestinal segments. Chyme osmolality increased linearly (p < 0.001) with salinity in the stomach and it decreased in all intestinal segments. Water fluxes were similar among salinities in the stomach, but they increased nearly fivefold (6.2 versus 27.3 ml g⁻¹ ingested DM) in the proximal intestine between 0 ppt and 35 ppt. An efflux of monovalent ions (Na⁺ and K⁺) increased linearly (p < 0.001) with salinity in the proximal intestine. An efflux of divalent ions (Ca²⁺ and Mg²⁺) increased curvilinearly (p < 0.001) with salinity in the middle intestine. Plasma osmolality and ion levels increased with salinity. Crude protein digestibility and protease activity decreased significantly with water salinity in the intestine. Our study highlights that when Atlantic salmon moves from freshwater to higher water salinity environments, drinking of saltwater does not interfere with hydration of feed in the stomach, but instead bypasses to the proximal intestine to aid in osmoregulatory water uptake. Therefore, we suggest that water ingestion in seawater fish is intended for osmoregulation rather than to aid digestion by liquefying chyme in the stomach.
Spawning manipulation, broodfish diet feeding and egg production in farmed Atlantic salmon
2024, Aquaculture
Atlantic salmon aquaculture relies on continuous supply of high quality eggs. Broodfish nutrition and manipulation of ovulation time (photoperiod and temperature) are key factors. The optimum feeding period with broodfish diet has not been investigated before. The present study examined how feeding period with broodfish diet (9 vs. 17 months) interacted with manipulation of ovulation time (early (Nov), normal (Dec), late (Feb)) on broodstock egg production capacity and egg quality in two-sea-winter female Atlantic salmon (∼12 kg). All groups were fed until June 2021 when they were transferred to tanks and starved until ovulation.
There were no measurable main or interaction effects of feeding period. Manipulation of ovulation gave several significant effects compared to normal ovulating females:
- 1.
  Early ovulating females had higher viscerosomatic index, smaller eggs with higher swelling rate (early 1.36, normal 1.27, late 1.23), and lower egg quality shown as reduced survival from fertilization to the eyed egg stage (mortality: early 11%, normal 5%, late 14%).
- 2.
  Late ovulating females: (i) were emaciated as shown by low condition factor calculated on gutted weight, and hepatosomatic and viscera indexes; (ii) had larger gonads caused by larger eggs; (iii) had reduced egg quality measured as elevated mortality from fertilization to first-feeding (eyed egg – first feeding: early 11%, normal 8%, late 23%).
- 3.
  All groups spawned a similar number of eggs per female.
The current results show that the feeding period with broodstock diet may be set to 9 months. This would make Atlantic salmon egg production more economical and environmentally sustainable. The results also show that manipulation of ovulation time reduce egg quality but not fecundity. Further research should investigate feeding periods with broodstock diet shorter than 9 months and determine the threshold for jeopardized fish welfare with respect to starvation time for manipulated late ovulating females.
Long term effects of smolt production strategy and early seawater phase rearing environment on mortality, growth, sexual maturation, and vertebra deformities in farmed Atlantic salmon (Salmo salar L.)
2023, Aquaculture
The life history of Atlantic salmon is plastic and determined by factors such as daylength and temperature. In aquaculture, artificial long days during smolt production maximize growth and allows for early sea-transfer, occurring between the first summer and autumn after hatching. However, the impact of such intensive rearing strategies on the salmon's welfare is not well understood. In this study, we follow underyearling (0+) juvenile salmon through two different smolt production regimes, either dietary induced seawater tolerance (fed with SuperSmolt®) under continuous light (LLS), or light-induced seawater tolerance, where for six weeks the photoperiod was lowered to 12 h light and 12 h darkness and then increased again to continuous light (LD-LL). Next, the LD-LL and LLS salmon were distributed into indoor seawater tanks where they experienced light and temperature conditions simulating either an August (AUG) or an October (OCT) sea transfer scenario lasting 2 months, after which all fish were transferred into a sea cage and reared there until reaching harvest size (10 months). Welfare parameters were mortality, growth, vertebra deformities (radiology), and sexual maturation. LLS grew faster than LD-LL smolts up until seawater transfer, while LD-LL post-smolts grew faster during the early seawater phase, resulting in equal harvest weights. The simulated AUG transfer gave higher harvest weights than the simulated OCT transfer regardless of smolt production strategy. Mortality during the first period in sea cages was higher in the LD-LL compared to LLS fish within the AUG scenario. At harvest, male sexual maturation was significantly higher in the LLS AUG (21%) group compared to the other groups (∼10%), while the occurrence of fish with vertebra deformities (1 ≥ deformed vertebrae) was highest among LD-LL fish within the AUG scenario (31%). Only the LD-LL fish had severely deformed individuals (fish with >10 deformed vertebrae): 2.8% in AUG and 5.6% in OCT. The present study shows that the incidence of male sexual maturation and vertebral deformities is lower in dietary- and photoperiod-induced smolts, respectively, by transferring them to seawater in autumn rather than summer. However, such a strategy could be expected to reduce the harvest weight of both LD-LL- and LLS-induced smolts.
Photoperiod and dietary treatment in freshwater modulate the short-term intestinal response to seawater in Atlantic salmon (Salmo salar)
2023, Aquaculture
Stimulation and timing of smoltification are essential for successful Atlantic salmon (Salmo salar) aquaculture. This study investigated intestinal responses during dietary and photoperiod manipulation in freshwater (FW) and after a subsequent seven days residence in seawater (SW). “Small” and “large” Atlantic salmon parr (∼40 g and ∼ 130 g respectively) were treated in FW for 12 weeks and thereafter transferred to SW for seven days. During the FW phase, fish underwent two different light conditions, 24 L:0D – 24 L (“LL-LL” groups) and 7 L:17D – 24 L (“SP-LL” groups) or fed with either regular feed (“LL-LL C" and “SP-LL C" groups) or feed enriched with a salt mix plus free tryptophan (“LL-LL + diet” and “SP-LL + diet” groups). We analyzed Na⁺/K⁺-ATPase (NKA) activity, tissue bioelectrical properties in Ussing chambers, and intestinal fluid composition. The NKA activity showed minor variations in relation to fish size, treatments, or intestinal region (anterior or posterior). Photoperiod modulated epithelial bioelectrical properties (I_sc and R_t) of the anterior and posterior intestine, particularly transepithelial resistance (R_t). Pharmacological experiments, targeting apical Na⁺/K⁺/2Cl⁻ (NKCC2) and Na⁺/Cl⁻ (NCC) co-transporters revealed intestinal region- and water salinity-dependent effects. In addition, stimulation of the intracellular cAMP with forskolin and IBMX showed intestinal region-, water salinity, and treatment-dependence responses with clear functional specialization of the anterior and posterior intestine. The intestinal fluid composition reflected the ability to process ingested SW and showed little variation in large fish. In summary, our data suggest a better pre-adaptation of the intestine during light-stimulated smoltification (SP-LL groups), and the combination of light and diet might give, in an industrial aquaculture setting, an advantage to smaller, but not larger smolts. Intestinal fluid composition in small fish can be used as an index of intestinal function and may act as a long-term performance proxy in SW Atlantic salmon.

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4 The Physiology of Smolting Salmonids

Publisher Summary

Comp. Biochem. Physiol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol., Suppl.

Aquaculture

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Gen. Comp. Endocrinol.

Comp. Biochem. Physiol. A

Aquaculture

Aquacultures

Aquaculture

Aquaculture

Gen. Comp. Endocrinol.

Aquaculture

Gen. Comp. Endocrinol.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Aquaculture

Comp Biochem. Physiol. A

Gen. Comp. Endocrinol.

Aquaculture

Aquaculture

J. Fish. Res. Board Can.

Inhibition of saltwater survival and Na+-K+-ATPase elevation in steelhead trout (Salmo gairdneri) by moderate water temperatures

Trans. Am. Fish. Soc.

Effects of castration on the smoltification of precocious male masu salmon (Oncorhynchus masou)

Bull. Jpn. Soc. Sci. Fish.

Healthy salmon at U.B.C. show expert he's wrong

Salinity preference, thyroid activity and the seaward migration of four species of Pacific salmon (Oncorhynchus)

J. Fish. Res. Board Can.

Factors in the diadromous migrations of fish

Symp. Zool. Soc. London

The effect of TSH and antithyroid substances on salinity preference and thyroid activity in juvenile Pacific salmon

Can. J. Zool.

Photoperiodic and endogenous control of the annual reproductive cycle in teleost fishes

Influence of parental smolt age and sea age on growth and smolting of hatchery-reared Atlantic salmon (Salmo salar)

Can. J. Fish. Aquat. Sci.

Étude comparée du métabolismé respiratoire du jeune Saumon sédentaire (parr) et migrateur (smolt)

C. R. Seances Soc. Biol. Ses. Fil.

Salt and water balance in rainbow trout (Salmo gairdneri) rapidly transferred from fresh water to sea water

J. Exp. Biol.

External morphology of the pink salmon, Oncorhynchus gorbuscha, introduced into Lake Superior

J. Fish. Res. Board Can.

Endocrinological studies on normal and abnormal salmon smoltification

Salmonid smoltification. Proceedings of a symposium sponsored by the Pacific sea grant advisory program and the California Sea Grant College Program

Aquaculture

Inhibition of saltwater survival and Na⁺-K⁺-ATPase elevation in steelhead trout (Salmo gairdneri) by moderate water temperatures