The impact of nutritional factors on the immune system in Atlantic salmon, Salmo salar L.

Abstract. Pancreas disease (PD) was induced by inoculating freshwater parr, Salmo salar L., with a homogenate of pooled tissues collected from four fish in the acute phase of disease. Pathological changes were observed in the liver and pancreas on day 4 post inoculation (PI) and in the heart on day 8 PI. Regeneration of necrotic acinar tissue was evident by day 8 PI. The infectious nature of PD was manifested by fish cohabiting with experimentally infected fish succumbing to PD after 13 days. The PD agent/agents retained its infectivity after filtration through a 0-2-μm filter.     

A genetic tool for evaluating male‐mediated stock introgression in Atlantic salmon

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Selective segregation in intraspecific competition between juvenile Atlantic salmon (Salmo salar) and brown trout (Salmo trutta)

Interactive segregation has been suggested as the ruling competition mechanism determining niche and niche segregation between juvenile Atlantic salmon (Salmo salar) and brown trout (Salmo trutta). Results from allopatry–sympatry observations of habitat use in both nature and in experiments were contrary to predictions derived from the interactive segregation hypothesis. Habitat use parameters under natural conditions such as distance to shore for Atlantic salmon parr were nearly identical in allopatric (mean ± SD; 3.2 ± 1.4 m) and sympatric (3.3 ± 1.4 m) situations. Occupied water depths largely reflected available water, but water depths <15 cm were avoided by salmon parr. Under experimental conditions, habitat use of allopatric salmon was density independent and salmon size had only minor effects, with smaller fish being more likely to occur in the shallow. Habitat use of salmon in sympatry with trout did not differ from allopatric salmon habitat use, and only salmon size had minor effects on depth choice – occurrence of trout or fish density had no effect. Allopatric trout was in general more frequent in the shallow habitat than salmon. Habitat use of sympatric trout was affected by the occurrence of salmon and trout size, resulting in a higher use of the shallow habitats for small trout. To conclude, selective segregation has a dominant role in salmon habitat use (not affected by trout occurrence), whereas a mixed situation occurs in trout habitat use with elements of interactive segregation when competing with Atlantic salmon (affected by salmon occurrence).     

Amoebic gill disease (AGD)-affected Atlantic salmon, Salmo salar L., are resistant to subsequent AGD challenge

There is inconsistent evidence of resistance of Atlantic salmon, Salmo salar L., to amoebic gill disease (AGD). Here, evidence is presented that demonstrates that Atlantic salmon exposed and subsequently challenged with AGD are more resistant than naïve control fish. Seventy‐three per cent of Atlantic salmon previously exposed to AGD survived to day 35 post‐challenge compared with 26% exposed to Neoparamoeba sp. for the first time, yet the gill pathology of surviving naïve control or previously exposed fish was not significantly different. Development of resistance to AGD is associated with anti‐Neoparamoeba sp. antibodies that were detectable in serum of 50% of surviving Atlantic salmon previously exposed to AGD. However, anti‐Neoparamoeba sp. antibodies were not detectable in cutaneous mucus of resistant fish. Increased resistance of Atlantic salmon after secondary Neoparamoeba sp. infection and detection of specific serum antibodies provides support for the development of a vaccine for AGD.     

Quality of raw and smoked fillets from clinically healthy Atlantic salmon,Salmo salar L., following an outbreak of pancreas disease (PD)

Pancreas disease (PD) is a viral disease of farmed salmonid fish, which causes huge economic losses. Pathological changes in skeletal muscle, pancreas and heart are hallmarks of PD. Stakeholders in the fish‐smoking industry have claimed that fillets from PD‐affected Atlantic salmon, Salmo salar L., are of poor quality. We therefore examined harvest‐ready, clinically healthy Atlantic salmon from a population of fish previously affected by PD. Histopathological changes in skeletal muscle tissues ranged from minor to severe. Fillet quality measurements showed that fish with severe skeletal muscle changes provided a paler raw fillet and a yellowish and harder cold‐smoked fillet than normal. PD had no significant effect on fillet gaping, bacteriological quality or off‐odour development during storage. An unexpected finding was a significant subendocardial fibrosis in 23% of the PD‐affected fish. The latter may indicate susceptibility to stress‐related heart failure.     

Some behavioural and ecological factors affecting distribution,biomass and production of juvenile Atlantic salmon

Observations were made in an experimental stream tank (total area 14.7 m²) on juvenile Atlantic salmon, Salmo salar L (parr), relating experimental observations to field observations, including the reported diurnal fasting behaviour of juvenile salmon at water temperatures <10 °C. Densities in the tank ranged from five to twenty parr, at water temperatures ranging from 4.6 °C to 15.8 °C. The wide channel of the stream tank, with mean water velocity of 18.8 cm·s^?1, was the preferred section, where territorial behaviour was observed. Biomass was regulated in the wide channel by territorial mosaics or by dominance hierarchies. Dominance hierarchies were reflected in coloration of the fish. Dominant salmon were generally in the wide channel. Densities of salmon parr (of mean fork length 10.2 cm) in the channel ranged from 0.84 m^?2 to 1.73 m^?2, with an average biomass of 14.2 g·m^?2. Growth was least at the 5.9 °C temperature treatment. In experiments at temperatures below 10 °C, feeding, dominance hierarchy and territorial behaviour were observed in daylight hours, contrary to the published literature. Interactions with other species may affect behaviour. Some observations were made on a closely related species, brown trout (Salmo trutta L.), a commonly cohabiting species in many systems. Trout displaced salmon from their preferred locations in the tank and were more aggressive than the salmon, reducing agonistic behaviour by the salmon. The commonest agonistic act shown by salmon was ‘charge’ and that by the trout was ‘approach’. Some field observations affecting behaviour and production are discussed.     

Do habitat measurements in the vicinity of Atlantic salmon (Salmo salar) parr matter?

Atlantic salmon, Salmo salar L., parr habitat characterisation is usually performed by in situ measures of key environmental variables taken at the exact fish location if the fishing gear allows precise pinpointing of this location, or in large sampling sections covering a river reach or mesohabitat, often ignoring variability in the immediate vicinity around individual fish. These data may be critically important in the development and validation of habitat preference models. The influences of seven increasing distances of measures, the variation of the number of considered measures and the depth of velocity measurement (bottom or 0.6 of the depth) in the calculations of HSI (Habitat Suitability Index) from a multiple‐experts fuzzy model of Atlantic salmon parr habitat were tested. When a parr was present, six measures collected in a 50‐cm radius around the fish to provide an average measure as input data and velocity measured at 60% of the depth gave the highest HSI values. These results show some potential for the use of an intermediate study scale, between micro‐ and mesohabitat, and questions how fish habitat conditions are currently measured.     

The immune response of Atlantic salmon, Salmo salar L., to the causative agent of bacterial kidney disease, Renibacterium salmoninarum

Abstract. Both under-yearling and post-yearling Atlantic salmon parr produced high agglutinating antibody titres in response to a single intraperitoneal injection of killed bacterial kidney disease (BKD) cells emulsified in. Freund's complete adjuvant (FCA), Low or no response was observed in animals injected with BKD cells in saline or in animals vaccinated by hyperosmotic immersion. Immunological duration was insufficient in fish vaccinated as under-yearling parr to provide protective immunity 2 years later when the fish had become smolts. Atlantic salmon post-yearling parr injected with BKD cells in FCA demonstrated a reduced prevalence of BKD lesions compared to control animals when both were observed as smolts 1 year after vaccination.     

Do changes in Atlantic salmon,Salmo salar L., fillet fatty acids following a dietary switch represent wash‐out or dilution? Test of a dilution model and its application

The fatty acid compositions of fish tissue lipids usually reflect those of the feed lipids, but few attempts have been made to predict the way in which the profiles change or assess the time required for the fatty acid profile to stabilize following a dietary change. The present focus on the influences of vegetable oils and fish oils on the fatty acid compositions and sensory attributes of fish fillets increases the interest in the ability to make such predictions. A dilution model was tested using data for the influences of feed oils (rape/linseed (V) vs. sand‐eel (F)) and dietary fat concentrations (ca. 30% (H) vs. ca. 20% (L)) on the body growth and fatty acid compositions of the fillets of Atlantic salmon, Salmo salar L., parr and post smolt. Fish given HV or LV feeds during freshwater rearing (mass increase from ca. 19 g to ca. 130 g) were switched to HF and LF feeds following parr–smolt transformation. The changes in fillet percentages of 18:1, 18:2 (n‐6) and 18:3 (n‐3) during 98 days of on‐growing in seawater (mass increase from ca. 130 g to ca. 380 g) conformed closely to predictions made on the basis of the dilution model. Model applications require information about the proportionate increase in fillet fat over time, but the relative changes in body mass can be used as a surrogate provided that both fillet yield (as a % of body mass) and fillet fat percentage change little over time. This is not the case for small salmon, but does seem to apply to larger salmon as they approach harvest size. This means that, for large salmon, ratios of changes in body mass can be substituted for ratios in the quantitative change in fillet fat without the introduction of a large error in the prediction of the change in fillet fatty acid profile following the introduction of a novel feed.     

In vitro passages impact on virulence of Saprolegnia parasitica to Atlantic salmon,Salmo salar L. parr

The effect of serial in vitro subculturing on three pathogenic strains of Saprolegnia parasitica was investigated. The isolates were passed through Atlantic salmon, Salmo salar L. parr, and then re‐isolated as single spore colonies. All strains caused infection. The isolate obtained from diseased fish served as a virulent reference culture and was designated ‘AP’ (‘activated through passage’). Successive subculturing was made by obtaining an inoculum from AP to produce the 2nd subculture and then passaged to the 3rd subculture (from the 2nd), until the 15th passage was obtained. Spores used to produce storage cultures were collected at passages 5, 10 and 15. The different passages of each strain were used to artificially infect Atlantic salmon parr. Morphological characterization of growth patterns was performed to observe differences occurring due to serial in vitro subculturing. Two of the strains declined in virulence after 15 successive in vitro subcultures, whereas one did not. This study is the first to investigate attenuation of virulence in Saprolegnia and whether or not isolates of S. parasitica should be passed through the fish host prior to challenge experiments. It reveals that some strains degenerate more rapidly than others when subjected to successive in vitro subculturing on glucose–yeast extract.     

Adiposity and growth of post-smolt Atlantic salmon Salmo salar L.

The long‐term adipose homeostasis seen in mammals gives rise to a ‘lipostatic’ model in which signals produced in proportion to fat stores serve to regulate energy intake. An extension of this predicts an impact of these signals on growth; downregulation of feeding in animals with increased adiposity should result in reduced growth. This was tested by monitoring fat deposition and growth in Atlantic salmon Salmo salar L. provided with feeds that differed in fat content. Salmon parr (mass c. 20 g) were fed either high‐ (H: 34%) or low‐fat (L: 22%) feeds, based on either fish (F) or vegetable (V) oils for 6 months to create groups of fish that differed in adiposity (10–12% and 5–7% body fat) at parr–smolt transformation (mass c. 130 g). Fish fed the high‐fat feeds deposited more body fat, and this was confirmed by measurement of fat concentrations in the fillet, viscera and remaining carcass. The fish were then grown‐on in sea water (c. 35 g L^?1, 8 °C, 24L:0D) for 14 weeks while being fed either high‐ or low‐fat feed formulated with fish oil to give the following treatments: HF→ H, HF→ L, LF→ L, LF→ H, HV→ H, HV→ L, LV→ L, LV→ H. Although fish exposed to the various feed treatments did not differ markedly in growth rate (SGR range 1–1.14% day^?1) over the 14 weeks of rearing in sea water, the results were in general agreement with predictions from the ‘lipostatic’ model, i.e. fish with the greatest fat reserves after the parr–smolt transformation grew more slowly than fish that were ‘leaner’ at this time. This suggests that adiposity, or ‘fatness’, may exert a negative feedback on feeding in salmon, thereby having an influence upon growth.     

Histology,immunocytochemistry and qRT‐PCR analysis of Atlantic salmon,Salmo salar L., post‐smolts following infection with infectious pancreatic necrosis virus (IPNV)

Infectious pancreatic necrosis (IPN) is a very serious viral disease in terms of its impact on production of Atlantic salmon, Salmo salar L., fry and post‐smolts. Post‐smolts of Atlantic salmon were injected with infectious pancreatic necrosis virus (IPNV) and cohabited with naive fish to produce natural infection. Cohabitant fish were sampled every 2 days, up to day 36 post‐infection (p.i.). From 90 cohabitant fish, 11 (12.2%) were positive by immunohistochemistry (IHC). The first detection of IPNV by IHC occurred on day 16 p.i. which coincided with the onset of mortality in this group. Besides the pancreas, the liver was found to be a key target organ for IPNV. For the first time, the virus was observed in the islets of Langerhans and in the kidney corpuscles of Stannius which suggests that the virus could affect the fish’s metabolism. The liver of two fish, which showed the most widespread presence of IPNV by IHC, had a pathology including focal necrosis and widespread presence of apoptotic hepatocytes, many of which did not stain for virus by IHC. Up‐regulation of cytokine gene expression was found only in the IHC‐positive (IHC+ve) fish and reflected the level of infection as determined by IHC positivity of the liver. In most fish, interferon (IFN), Mx, γIFN and γIP were up‐regulated in liver and kidney, while only IFN and Mx were up‐regulated in gill. IL1β and TNFα were not induced in any tissue. The gill showed variable levels of constitutive expression of IL1β and γIFN. The two fish with liver pathology had the highest level of IFN expression, especially relative to the level of Mx expression, in the liver compared with the other IHC+ve fish which did not have a liver pathology. The results suggest that following widespread infection of hepatocytes, the cells may over‐produce IFN, resulting in apoptosis of neighbouring cells with subsequent death from liver failure.     

An additional life-history tactic of masu salmon: Migration of parr to coastal habitats

Alternative life-history tactics of masu salmon Oncorhynchus masou are well documented. Subsequent to the freshwater parr stage (age ≥ 1 + years), an anadromous form migrates to the sea after smolting, while a resident form matures without seaward migration. In addition to this typical migratory dimorphism, anecdotal reports based on field observations have indicated that some underyearling masu salmon use estuarine waters. However, no empirical evidence indicates saltwater utilisation and subsequent survival in the early parr stage. Here, we used otolith microchemistry to examine whether a portion of masu salmon parr in northern Japan enters coastal habitats. The otolith Sr:Ca ratios of most juveniles collected from six rivers had consistently low values, indicating that masu salmon parr inhabiting these rivers stay only in freshwater. In contrast, in individuals from a steep-gradient river the Sr:Ca ratios increased at about a 200-µm distance from the otolith core. These results suggest that some masu salmon parr might use brackish water or sea water temporarily. In addition, three masu salmon parr were found in another steep river where a culvert located only ten metres from the river mouth completely blocked upstream migration for spawning. The Sr:Ca ratios in these fish increased at about >200 µm from the otolith core, indicating the parr had immigrated to the non-natal river from the sea. Such flexible behaviour at an early life stage may contribute to the spatial expansion of masu salmon, and the movement could moreover help to stabilise its population dynamics.     

Physiological responses to continuous swimming in wild salmon (Salmo salar L.) parr and smolt

Wild salmon (Salmo salar) parr and smolt were forced to swim against constant flow (50 cm.s^–1) for 8 hours. Physiological properties describing the hormonal status, the energy metabolism and the ionic and osmotic balance of fish were measured from the fish prior to and at the end of the swimming test.Plasma cortisol levels were elevated in response to enforced swimming; the response of the smolt was clearly greater than that of the parr. Plasma thyroxine concentration increased in the parr but stayed at the initial level in the smolts. The parr consumed much of their coelomic fat, but the glycogen stores stayed nearly constant. The smolts had very low fat stores, and the glycogen stores were depleted in the test. The ionic and osmotic balance of the parr was stable in the test, but in smolts, the plasma Cl^–1 and osmotic concentrations decreased and muscle moisture increased.The results indicate that downstream migration smolts have markedly lower physiological capacity for continuous swimming than parr.     

Selective precipitation reaction: a novel diagnostic test for tissue pathology in Atlantic salmon,Salmo salar,infected with salmonid alphavirus (SAV3)

While investigating biomarkers for infection with salmonid alphavirus (SAV), the cause of pancreas disease (PD), a selective precipitation reaction (SPR) has been discovered in serum which could be an on‐farm qualitative test and an in‐laboratory quantitative assay for health assessments in aquaculture. Mixing serum from Atlantic salmon, Salmo salar, with SAV infection with a sodium acetate buffer caused a visible precipitation which does not occur with serum from healthy salmon. Proteomic examination of the precipitate has revealed that the components are a mix of muscle proteins, for example enolase and aldolase, along with serum protein such as serotransferrin and complement C9. The assay has been optimized for molarity, pH, temperature and wavelength so that the precipitation can be measured as the change in optical density at 340 nm (Δ₃₄₀). Application of the SPR assay to serum samples from a cohabitation trial of SAV infection in salmon showed that the Δ₃₄₀ in infected fish rose from undetectable to a maximum at 6 weeks post‐infection correlating with histopathological score of pancreas, heart and muscle damage. This test may have a valuable role to play in the diagnostic evaluation of stock health in salmon.     

Road culvert restoration expands the habitat connectivity and production area of juvenile Atlantic salmon in a large subarctic river system

The effects of restoration of impassable road culverts on the distribution of juvenile Atlantic salmon, Salmo salar L., were evaluated in seven small tributaries of the subarctic River Teno system, northernmost Finland/Norway. Restoration enabled the passage of juvenile salmon through the culverts and increased the distribution area of salmon parr in the seven streams by tens or hundreds of metres, depending on the natural slope of the tributary with a total of ≈1 km new area for ascending juveniles. Areas upstream of the culverts were colonised after varying number of years, mostly 2–3, following restoration. Age‐1 and age‐2 parr were the first salmon age groups entering the new territory after removal of the migration barrier. Although the restoration measures were conducted at the downstream outlet area of the culverts only, the connectivity was improved and increased the production area accessible to juvenile salmon. Such removal of migration barriers and securing habitat connectivity by passable culverts should be taken into account in environmental management strategies of river systems safeguarding the essential habitats of salmonid fish.     

Effects of dietary vitamin C on growth and parr-smolt transformation in Atlantic salmon, Salmo salar L.

Atlantic salmon (Salmo salar) parr were fed fish meal based pelleted diets supplemented with graded levels of ascorbate-2-monophosphate (AP), equivalent to 0, 20, 60 and 1000 mg ascorbic acid (AA) kg”¹ throughout smoltification on a continuous light regime from February to June. No differences were observed in growth rate and body length distribution between the dietary regimes. The condition factor and the hepatosomatic index were somewhat elevated in fish fed no vitamin C throughout the smoltification, which can reflect changes in lipid metabolism in fish with suboptimal vitamin C nutrition. Sea water challenge tests (exposure to sea water with salinity of 34 gL^?1 and ambient temperature for 24 h) performed monthly did not reveal differences attributed to the vitamin C status, as measured by mortality, serum chloride and cortisol concentrations, haematological parameters and liver and head kidney ascorbate concentrations after 24 h. Elevated serum cortisol concentrations most probably reflected stress in the challenge tests, and some lower concentrations in fish fed high vitamin C levels may indicate a certain stress-ameliorating effect. The present results do not, however, support the anticipation of increased requirement of dietary vitamin C above the minimum requirement during smoltification in Atlantic salmon.     

Development of a reproducible infectious pancreatic necrosis virus challenge model for Atlantic salmon, Salmo salar L.

Atlantic salmon smolts, previously unexposed to infectious pancreatic necrosis virus (IPNV), were placed into tanks of sea water at 10 °C. After 4 weeks, 40 fish were injected intraperitoneally (i.p.) with homogenized and filter‐sterilized kidney material obtained from salmon with clinical IPN in a marine farm in Shetland. The injected fish were cohabited with 40 untreated fish. Mortalities began in the injected fish on day 7 and reached a peak of 48% on day 14. In the cohabitation group, mortalities began on day 14 and reached a peak of 70% on day 27. The IPNV in the Shetland kidney homogenate was cultured in Chinook salmon embryo (CHSE) cells and passed twice. This cultured virus was injected i.p. into fish at various doses ranging from 10 to 10⁷ TCID₅₀ fish^?1 4 weeks after seawater transfer. Challenge tanks contained 30 injected fish and 30 cohabitees. Mortality rates and levels were dose‐dependent. The highest dose used resulted in a similar mortality pattern as obtained with a similar dose of the Shetland kidney homogenate, indicating that virulence was retained after two passes in tissue culture. Even with the lowest dose, mortality reached 12% in the injected group and 23% in the cohabitees. The IPNV titres were high (10⁶?10⁹ i.u. g^?1 kidney) in fish which died during the experiment and low (<10⁵ i.u. g^?1 kidney) or undetectable in surviving fish. The cultured virus (pass 3) was used in a challenge model where the population density of fish in the tanks was high (50 injected and 50 cohabitees) or low (15 injected and 15 cohabitees). In the high stocking density tank, mortalities peaked at about 35% in the injected group and at 52% in the cohabitees. In the low stocking density tank, mortalities peaked at about 40% in the injected fish but no mortality occurred in the cohabitees. However, IPNV was detected (up to 10⁴ i.u. g^?1 kidney) in 82% of cohabitees sampled on day 30. These data suggest that lethal lateral transmission of the virus is dependent on the infectious pressure from the injected group. A further trial was conducted to investigate the effect of time post‐seawater transfer on the susceptibility of post‐smolts to IPN. Groups of fish were challenged every 2 weeks from week 0–10. Few mortalities occurred at week 0 and virus titres were high in these fish. Most survivors became carriers, some with titres >10⁶ i.u. IPNV g^?1 kidney. From 2 to 10 weeks after seawater transfer, mortalities in both injected and cohabitees were substantial with viral titres >10⁷ i.u. g^?1 kidney. Survivors had lower titres and in many virus was undetectable. Throughout the experiments, moribund fish were sampled for histology and all showed typical IPN histopathology.     

High marine survival rates of sea‐ranched Atlantic salmon smolts (Salmo salar) that had previously matured as male parr

Abstract The growth and recapture rates of Atlantic salmon, Salmo salar L., smolts that had previously matured as parr were compared with those of immature siblings in a sea‐ranching experiment in western Norway. The smolts were the offspring of three river populations. They were individually tagged, transferred to cages in a small bay where estuarine salinity gradients had been established and released on four dates from mid‐May to early June after either 3 or 7 days of acclimatisation. The previously mature male parr (PMMP) were smaller than their siblings before release, but performed much better during their time in the sea. As grilse, they reached sizes comparable with the formerly immature fish, and their recapture rate was more than four times higher (8.6 vs 2.1%). This difference decreased somewhat during the following years because 0.85% of the immature fish and only 0.1% of PMMP were recaptured as multi‐sea‐winter salmon. The highly successful marine performance of the PMMP demonstrated that this life history strategy may be more flexible than previously believed.