Erythrocytic inclusion body syndrome virus in wild Atlantic salmon, Salmo salar L

An investigation was undertaken to establish aspects of the epizootiology of erythrocytic inclusion bodies in wild Atlantic salmon, Salmo salar L., in Scotland. From 1992 to 1995, adult and juvenile salmon, from Scottish rivers, were screened for the presence of erythrocytic inclusion bodies and haematological parameters measured. The nature of the inclusion bodies was assessed through transmission electron microscopy, negative-staining and blood smear-staining techniques and was demonstrated to be viral in origin with characteristics similar to a member of the family Togaviridae. Specifically, these were a viral genome of single-stranded RNA, spherical virion morphology with an icosahedral core, average size of 70 nm and a buoyant density of 1.15-1.20 g cm(-3). The cytoplasmic inclusions were either large, single inclusions (1-2 microm) or smaller multiple inclusions (0.5-1 microm). A total of 4.2% (n=48) and 27.7% (n=213) of the parr and adult salmon, respectively, were positive for the presence of the inclusions. The intensity of the inclusions, when present, varied from light in parr to moderate and heavy in adults, when graded according to the number of inclusions per field of view. Neither haematological variations nor clinical disease was associated with the presence or absence of viral inclusions.     

Cardiomyopathy syndrome in Atlantic salmon Salmo salar L.: A review of the current state of knowledge

Cardiomyopathy syndrome (CMS) is a severe cardiac disease affecting Atlantic salmon Salmo salar L. The disease was first recognized in farmed Atlantic salmon in Norway in 1985 and subsequently in farmed salmon in the Faroe Islands, Scotland and Ireland. CMS has also been described in wild Atlantic salmon in Norway. The demonstration of CMS as a transmissible disease in 2009, and the subsequent detection and initial characterization of piscine myocarditis virus (PMCV) in 2010 and 2011 were significant discoveries that gave new impetus to the CMS research. In Norway, CMS usually causes mortality in large salmon in ongrowing and broodfish farms, resulting in reduced fish welfare, significant management‐related challenges and substantial economic losses. The disease thus has a significant impact on the Atlantic salmon farming industry. There is a need to gain further basic knowledge about the virus, the disease and its epidemiology, but also applied knowledge from the industry to enable the generation and implementation of effective prevention and control measures. This review summarizes the currently available, scientific information on CMS and PMCV with special focus on epidemiology and factors influencing the development of CMS.     

Viral co‐infections in farmed Atlantic salmon,Salmo salar L., displaying myocarditis

Several different viruses have been associated with myocarditis‐related diseases in the Atlantic salmon aquaculture industry. In this study, we investigated the presence of PMCV, SAV, PRV and the recently identified Atlantic salmon calicivirus (ASCV), alone and as co‐infections in farmed Atlantic salmon displaying myocarditis. The analyses were performed at the individual level and comprised qPCR and histopathological examination of 397 salmon from 25 farms along the Norwegian coast. The samples were collected in 2009 and 2010, 5–22 months post‐sea transfer. The study documented multiple causes of myocarditis and revealed co‐infections including individual fish infected with all four viruses. There was an overall correlation between lesions characteristic of CMS and PD and the presence of PMCV and SAV, respectively. Although PRV was ubiquitously present, high viral loads were with a few exceptions, correlated with lesions characteristic of HSMI. ASCV did not seem to have any impact on myocardial infection by PMCV, SAV or PRV. qPCR indicated a negative correlation between PMCV and SAV viral loads. Co‐infections result in mixed and atypical pathological changes which pose a challenge for disease diagnostic work.     

Presence of anti-Neoparamoeba sp. antibodies in Tasmanian cultured Atlantic salmon, Salmo salar L

Previous studies have indicated that when Atlantic salmon, Salmo salar L., are exposed to Neoparamoeba sp. the fish produce anti-Neoparamoeba sp. antibodies. It appears unlikely that these antibodies elicit any specific protection against amoebic gill disease (AGD) as fish with demonstrable activities have been affected by AGD. Experiments were conducted on Atlantic salmon cultured throughout Tasmania to assess the natural production of antibodies towards Neoparamoeba sp. Fish were sampled from areas where AGD was prevalent and from areas where there had been no reported cases. An enzyme-linked immunosorbent assay (ELISA) was used to measure anti-Neoparamoeba sp. antibody activities in serum. All fish from sea water had antibody activities greater than the negative control fish, including fish from areas with no reported cases of AGD. Time trial samples indicated that time after transfer to sea water did not appear to be a significant (P > 0.05) factor in antibody activity, however location was (P < 0.05). There was no agreement (corrected kappa value, 0.16) between the ELISA result and the isolation of Neoparamoeba sp. from the gills of the same fish. The results suggest that Atlantic salmon in seawater culture in Tasmania produce anti-Neoparamoeba sp. antibodies regardless of infection history, suggesting the presence of Neoparamoeba sp. in the environment.     

Effects of temperature on amoebic gill disease development: Does it play a role?

A relationship between increasing water temperature and amoebic gill disease (AGD) prevalence in Atlantic salmon (Salmo salar) has been noted at fish farms in numerous countries. In Scotland (UK), temperatures above 12°C are considered to be an important risk factor for AGD outbreaks. Thus, the purpose of this study was to test for the presence of an association between temperature and variation in the severity of AGD in Atlantic salmon at 10 and 15°C. The results showed an association between temperature and variation in AGD severity in salmon from analysis of histopathology and Paramoeba perurans load, reflecting an earlier and stronger infection post‐amoebae exposure at the higher temperature. While no significant difference between the two temperature treatment groups was found in plasma cortisol levels, both glucose and lactate levels increased when gill pathology was evident at both temperatures. Expression analysis of immune‐ and stress‐related genes showed more modulation in gills than in head kidney, revealing an organ‐specific response and an interplay between temperature and infection. In conclusion, temperature may not only affect the host response, but perhaps also favour higher attachment/growth capacity of the amoebae as seen with the earlier and stronger P. perurans infection at 15°C.     

Response of juvenile Atlantic salmon, Salmo salar, to the introduction of salmon carcasses in upland streams

Abstract  The role of nutrients in the production of Atlantic salmon, Salmo salar L., in oligotrophic upland catchments is poorly understood. Atlantic salmon carcasses were introduced to 12 upland streams in the River Conon catchment, Scotland, UK, to assess potential nutrient limitation and evaluate a potential role for migratory Atlantic salmon in nutrient import. The objective was to test the hypothesis that nutrient supplementation would increase juvenile Atlantic salmon biomass. Streams received one of six treatment levels up to a maximum of one carcass per 15 m² of wetted area with duplicates at each level, and study areas were sampled to measure salmon biomass in treated and reference reaches. There was a significant positive relationship between treatment addition level and response of juvenile salmon biomass. At higher carcass addition levels, salmon biomass in treatment sections was approximately twice that in paired reference sections. The results are discussed in the light of management methods in upland regions and the likely role of cultural oligotrophication in suppressing current levels of salmon production.     

Isolation of salmon pancreas disease virus (SPDV) from farmed Atlantic salmon, Salmo salar L., in Scotland

A toga-like virus was recently isolated in the present authors' laboratory from Atlantic salmon during an outbreak of PD in Ireland (Nelson, McLoughlin, Rowley, Platten & McCormick 1995). When inoculated into Atlantic salmon post-smolts, this virus, known as salmon pancreas disease virus (SPDV), caused pathological changes in the pancreas, heart and skeletal muscle which were indistinguishable from those observed in natural outbreaks of PD (McLoughlin, Nelson, Rowley, Cox & Grant 1996). In 1996 a serological survey was carried out to determine the presence and distribution of antibodies to SPDV in Irish, Scottish and Norwegian farm-reared Atlantic salmon (McLoughlin, Rowley & Doherty 1998). The results of this survey indicated that SPDV is present in the major European salmon-producing countries. The present paper describes the first isolation of SPDV from farm-reared, PD-affected Atlantic salmon in Scotland.     

Epitheliocystis in Atlantic salmon,Salmo salar L., farmed in fresh water in Ireland is associated with ‘Candidatus Clavochlamydia salmonicola’ infection

Intracellular inclusions containing chlamydia‐like organisms are frequently observed in the gill epithelial cells of Atlantic salmon, Salmo salar L., cultured in fresh water in Ireland. In this study, the causative agent was identified in four separate freshwater sites, using 16s rRNA sequencing, as ‘Candidatus Clavochlamydia salmonicola’. Histopathology and real‐time (RT) PCR were used to further assess infections. The prevalence of infection ranged from 75–100% between sites and infection intensity was highly variable. No significant lesions were associated with these infections. As a diagnostic tool, RT‐PCR proved marginally more sensitive than histopathology. The fate of ‘Candidatus Clavochlamydia salmonicola’ in Atlantic salmon post‐seawater transfer was investigated in a 12‐week marine longitudinal study. Both RT‐PCR and histopathological examination indicate that the organism disappears from the gills 4–6 weeks post‐transfer.     

Salmon gill poxvirus,a recently characterized infectious agent of multifactorial gill disease in freshwater‐ and seawater‐reared Atlantic salmon

Gill diseases cause considerable losses in Norwegian salmon farming. In 2015, we characterized salmon gill poxvirus (SGPV) and associated gill disease. Using newly developed diagnostic tools, we show here that SGPV infection is more widely distributed than previously assumed. We present seven cases of complex gill disease in Atlantic salmon farmed in seawater and freshwater from different parts of Norway. Apoptosis, the hallmark of acute SGPV infection, was not easily observed in these cases, and qPCR analysis was critical for identification of the presence of SGPV. Several other agents including Costia‐like parasites, gill amoebas, Saprolegnia spp. and bacteria were observed. The studied populations experienced significant mortalities, which increased to extreme levels when severe SGPV infections coincided with smoltification. SGPV infection appears to affect the smoltification process directly by affecting the gills and chloride cells in particular. SGPV may be considered a primary pathogen as it was often found prior to identification of complex gill disease. It is hypothesized that SGPV‐induced gill damage may impair innate immunity and allow invasion of secondary invaders. The distinct possibility that SGPV has been widely overlooked as a primary pathogen calls for extended use of SGPV qPCR in Atlantic salmon gill health management.     

Aeromonas salmonicida infects Atlantic salmon (Salmo salar) erythrocytes

Aeromonas salmonicida subsp. salmonicida (hereafter A. salmonicida) is the aetiological agent of furunculosis in marine and freshwater fish. Once A. salmonicida invade the fish host through skin, gut or gills, it spreads and colonizes the head kidney, liver, spleen and brain. A. salmonicida infects leucocytes and exhibits an extracellular phase in the blood of the host; however, it is unknown whether A. salmonicida have an intraerythrocytic phase. Here, we evaluate whether A. salmonicida infects Atlantic salmon (Salmo salar) erythrocytes in vitro and in vivo. A. salmonicida did not kill primary S. salar erythrocytes, even in the presence of high bacterial loads, but A. salmonicida invaded the S. salar erythrocytes in the absence of evident haemolysis. Naïve Atlantic salmon smolts intraperitoneally infected with A. salmonicida showed bacteraemia 5 days post‐infection and the presence of intraerythrocytic A. salmonicida. Our results reveal a novel intraerythrocytic phase during A. salmonicida infection.     

Heart and skeletal muscle inflammation in Atlantic salmon, Salmo salar L: a new infectious disease

Heart and skeletal muscle inflammation (HSMI) is a disease syndrome of unknown aetiology first observed in farmed Atlantic salmon, Salmo salar, in 1999. In the present study we have demonstrated for the first time that HSMI is an infectious disease. It was induced in Atlantic salmon post-smolts after injection with tissue homogenate from farmed Atlantic salmon previously diagnosed with HSMI. The lesions were also induced in cohabitating salmon given a corresponding injection without tissue homogenate. Six weeks post-challenge the fish that had been injected with tissue homogenate developed a serious epicarditis and myocarditis with mononuclear cell infiltrations in compact and spongy layers of the heart. Similar lesions were found in cohabitants after 10 weeks. The lesions were consistent with samples from field outbreaks of HSMI. No lesions were found in control fish. A viral aetiology is strongly suggested, as no difference in disease induction between an inoculum containing antibiotics and a non-treated inoculum was found. Further investigations are required in order to make conclusions regarding the cause and pathogenesis of HSMI.     

Prevalence of piscine orthoreovirus and salmonid alphavirus in sea‐caught returning adult Atlantic salmon (Salmo salar L.) in northern Norway

Heart and skeletal muscle inflammation (HSMI) caused by piscine orthoreovirus (PRV) and pancreas disease (PD) caused by salmonid alphavirus (SAV) are among the most prevalent viral diseases of Atlantic salmon farmed in Norway. There are limited data about the impact of disease in farmed salmon on wild salmon populations. Therefore, the prevalence of PRV and SAV in returning salmon caught in six sea sites was determined using real‐time RT‐PCR analyses. Of 419 salmon tested, 15.8% tested positive for PRV, while none were positive for SAV. However, scale reading revealed that 10% of the salmon had escaped from farms. The prevalence of PRV in wild salmon (8%) was significantly lower than in farm escapees (86%), and increased with fish length (proxy for age). Sequencing of the S1 gene of PRV from 39 infected fish revealed a mix of genotypes. The observed increase in PRV prevalence with fish age and the lack of phylogeographic structure of the virus could be explained by virus transmission in the feeding areas. Our results highlight the need for studies about the prevalence of PRV and other pathogens in Atlantic salmon in its oceanic phase.     

Maintenance ration, protein synthesis capacity, plasma insulin and growth of Atlantic salmon (Salmo salar L.) with genetically different trypsin isozymes

Growth was found to be associated with the changes of trypsin activity in the pyloric caecal tissues and the level of plasma insulin in Atlantic salmon (Salmo salar L.). A decrease in trypsin activity accompanied by an increase in plasma insulin was detected one month before an enhanced growth was observed. There were significant relationships between weight specific consumption rate, plasma insulin levels and fish growth. The correlation of weight specific consumption rate was higher with growth rate (R²=0.7, p<0.0001) than with plasma insulin concentration (R²=0.4, p<0.0001).When the comparison was made between Atlantic salmon carrying and lacking the trypsin variant TRP-2*92, the fish with the variant had lower maintenance ration (p<0.05), higher capacity for protein synthesis in the white muscle (p<0.02), and a greater ability to utilize the feed at a restricted ration than the fish without the variant. In Atlantic salmon lacking the variant, both plasma insulin concentrations and growth rates were significantly lower (p<0.05) in the fish fed 0.5% bw day^–1 than those fed 1% bw day^–1. Whilst the growth rates of TRP-2*92 salmon fed the different rations became similar one month after similar levels of plasma insulin were observed between them. The TRP-2*92 salmon may be defined as a high protein growth efficiency fish with low protein turnover rate.Genetic variation in trypsin isozyme pattern affects feed utilization, plasma insulin levels and growth in Atlantic salmon.     

Variation in semen production of farmed Atlantic salmon and rainbow trout

The variation in semen production among farmed Atlantic salmon (Salmo salar) and rainbow trout (Salmo gairdneri) has been studied. Both species were stripped at weekly intervals, the Atlantic salmon four times and the rainbow trout three times.The individual variation in volume of semen was very high, particularly in rainbow trout. The total volume of semen obtained was 137 ml (20 ml/kg body weight) in Atlantic salmon and 23 ml (5 ml/kg body weight) in rainbow trout. The intraclass correlation for volume of semen was estimated at 0.73 in Atlantic salmon and at 0.59 in rainbow trout. The correlations between volume of semen and body size (weight and length) were all positive. They were all significant and medium in Atlantic salmon whereas in rainbow trout they were all low and significant only for volume of semen at first stripping.The number of males needed to supply the Norwegian fish farming industry with semen is discussed. It is concluded that the possibility of disseminating genetic improvement throughout the whole population of farmed Atlantic salmon and rainbow trout by transport of semen from selected males is considerable.     

Heritability of mortality in response to a natural pancreas disease (SPDV) challenge in Atlantic salmon,Salmo salar L., post‐smolts on a West of Ireland sea site

Pancreas disease (PD) is an economically important disease of European farmed Atlantic salmon. It can cause significant losses because of morbidity, mortality and reduced production. The disease is caused by an alphavirus, known as salmon PD virus (SPDV) or salmonid alphavirus subtype 1 in Ireland. To examine whether it is possible to improve the natural resistance of Atlantic salmon to SPDV by selective breeding, 6000 genotyped, tagged, pedigreed fish from 150 full‐sib families were exposed to a natural challenge during 2005 in a sea cage on a commercial salmon farm in the West of Ireland. Histopathological and serological examination was performed weekly on a proportion of all moribund fish to determine the onset of the infection and the likely cause of death. Heritabilities and genetic correlations are presented for resistance to a natural PD challenge and smolt input weight. The results indicate that the susceptibility of salmon to SPDV could be reduced by selective breeding based on the survival in a natural challenge to the virus.     

The effect of dietary chitin on growth and nutrient digestibility in farmed Atlantic cod,Atlantic salmon and Atlantic halibut

The effect of adding 0%, 1%, 2% and 5% chitin from prawn shells in the diets for Atlantic cod, Atlantic halibut and Atlantic salmon on growth was investigated. Nutrient digestibility and feed utilization was investigated in salmon and cod. Atlantic cod grew from 186 ± 29 to 383 ± 78 g (N = 960) over 13 weeks. Dietary chitin had no effect on length, weight, condition, liver size or specific growth rate (SGR). The apparent digestibility (ADC) for protein ranged from 84.7% to 86.5%, lipid between 88.8% and 93.1% and dry matter from 96.1% to 96.6%. Feed utilization varied between 1.08 and 1.11 and was not correlated with dietary chitin content. Atlantic salmon tripled their weight from 199 ± 9 to 615 ± 75 g (N = 480) during the 13 weeks. High inclusions of chitin (>1%) reduced both growth rate and condition. Protein and lipid ADC was negatively correlated with dietary chitin. Feed utilization ranged between 0.86 and 0.90 and was not significantly affected by dietary chitin. Faecal protein increased significantly with increasing dietary chitin, while faecal dry matter and lipid did not. Individually tagged Atlantic halibut grew from 1300 ± 470 to 2061 ± 714 g (N = 70) during 6 months. Individual growth rates varied within each group from being slightly negative to 0.81%·day^?1. Diet had no significant effect on growth rates. Atlantic cod and Atlantic halibut seems unaffected by up to 5% chitin additions in the diet, while chitin >1% of diet negatively affects growth and nutrient utilization in Atlantic salmon.     

Alphavirus infections in salmonids--a review

The first alphavirus to be isolated from fish was recorded in 1995 with the isolation of salmon pancreas disease virus from Atlantic salmon, Salmo salar L., in Ireland. Subsequently, the closely related sleeping disease virus was isolated from rainbow trout, Oncorhynchus mykiss (Walbaum), in France. More recently Norwegian salmonid alphavirus (SAV) has been isolated from marine phase production of Atlantic salmon and rainbow trout in Norway. These three viruses are closely related and are now considered to represent three subtypes of SAV, a new member of the genus Alphavirus within the family Togaviridae. SAVs are recognized as serious pathogens of farmed Atlantic salmon and rainbow trout in Europe. This paper aims to draw together both historical and current knowledge of the diseases caused by SAVs, the viruses, their diagnosis and control, and to discuss the differential diagnosis of similar pathologies seen in cardiomyopathy syndrome and heart and skeletal muscle inflammation of Atlantic salmon.     

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.     

Interactions between naturalised exotic salmonids and reintroduced Atlantic salmon in a Lake Ontario tributary

Abstract – Atlantic salmon (Salmo salar) was once native to Lake Ontario, however, its numbers rapidly declined following colonisation by Europeans and the species was extirpated by 1896. Government agencies surrounding Lake Ontario are currently undertaking a variety of studies to assess the feasibility of reintroducing Atlantic salmon. We released hatchery‐reared adult Atlantic salmon into a Lake Ontario tributary to examine spawning interactions between this species and fall‐spawning exotic salmonids found in the same stream. Chinook salmon, coho salmon and brown trout were observed interacting with spawning Atlantic salmon in nearly one‐quarter of our observation bouts, with chinook salmon interacting most frequently. Whereas a previous investigation found that chinook salmon caused elevated agonistic behaviour and general activity by spawning Atlantic salmon, the present study found that interspecific courtship was the most common form of exotic interaction with spawning Atlantic salmon. In particular, we observed precocial male Chinook salmon courting female Atlantic salmon and defending the female against approach by male Atlantic salmon. We discuss the potential implications of these interactions on the Lake Ontario Atlantic salmon reintroduction programme.