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

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Potential disease interaction reinforced: double-virus-infected escaped farmed Atlantic salmon,Salmo salar L., recaptured in a nearby river

The role of escaped farmed salmon in spreading infectious agents from aquaculture to wild salmonid populations is largely unknown. This is a case study of potential disease interaction between escaped farmed and wild fish populations. In summer 2012, significant numbers of farmed Atlantic salmon were captured in the Hardangerfjord and in a local river. Genetic analyses of 59 of the escaped salmon and samples collected from six local salmon farms pointed out the most likely source farm, but two other farms had an overlapping genetic profile. The escapees were also analysed for three viruses that are prevalent in fish farming in Norway. Almost all the escaped salmon were infected with salmon alphavirus (SAV) and piscine reovirus (PRV). To use the infection profile to assist genetic methods in identifying the likely farm of origin, samples from the farms were also tested for these viruses. However, in the current case, all the three farms had an infection profile that was similar to that of the escapees. We have shown that double-virus-infected escaped salmon ascend a river close to the likely source farms, reinforcing the potential for spread of viruses to wild salmonids.     

Early marine survival and movements of escaped Atlantic salmon Salmo salar L. juveniles from a land‐based smolt farm during autumn

The aim of this study was to examine early marine survival and movements of simulated escaped Atlantic salmon Salmo salar L. pre‐smolt and smolt from a commercial smolt farm during autumn. One‐third of the pre‐smolt most likely died in the immediate vicinity of the release location, whereas the corresponding mortality for smolts was lower (8.5%) during the 5‐week study period. The surviving pre‐smolt left the farm area after 2–3 days, predominantly along the shore. In contrast, most of the surviving smolts left the farm area during the first day and 54% seemed to move away from the shore and adopt a more pelagic movement pattern than pre‐smolt. The number of surviving fish recorded in the fjord decreased throughout the study period, possibly due to a combination of fish migrating out of the fjord or undetected mortality. Compared with existing knowledge on migration of released farmed smolts during spring, our results indicate less directional and slower movement rates during autumn. Only two of the tagged fish were detected upstream in the rivers following release. A rapid dispersion of escapees indicates that the potential for recapturing escapees is limited unless recapture efforts are initiated immediately after escape. Hence, there is a need for development of technology that detects and prevents escapees to enter the sea.     

A historical review of the key bacterial and viral pathogens of Scottish wild fish

Thousands of Scottish wild fish were screened for pathogens by Marine Scotland Science. A systematic review of published and unpublished data on six key pathogens (Renibacterium salmoninarum, Aeromonas salmonicida, IPNV, ISAV, SAV and VHSV) found in Scottish wild and farmed fish was undertaken. Despite many reported cases in farmed fish, there was a limited number of positive samples from Scottish wild fish, however, there was evidence for interactions between wild and farmed fish. A slightly elevated IPNV prevalence was reported in wild marine fish caught close to Atlantic salmon, Salmo salar L., farms that had undergone clinical IPN. Salmonid alphavirus was isolated from wild marine fish caught near Atlantic salmon farms with a SAV infection history. Isolations of VHSV were made from cleaner wrasse (Labridae) used on Scottish Atlantic salmon farms and VHSV was detected in local wild marine fish. However, these pathogens have been detected in wild marine fish caught remotely from aquaculture sites. These data suggest that despite the large number of samples taken, there is limited evidence for clinical disease in wild fish due to these pathogens (although BKD and furunculosis historically occurred) and they are likely to have had a minimal impact on Scottish wild fish.     

Relationship between sea lice levels on sea trout and fish farm activity in western Scotland

The relationship between aquaculture and infestations of sea lice on sea trout, Salmo trutta L., is controversial. Here, the association between sea lice infestations on wild sea trout and characteristics of local Atlantic salmon, Salmo salar L., farms were investigated using data collected on the Scottish west coast. The proportion of sea trout with louse burdens above a critical level was positively related to the fork length of the sea trout and the mean weight of salmon on the nearest fish farm, and negatively related to the distance to that farm. The distance to the nearest fish farm did not influence the probability of infestations above the critical level beyond 31 km although there was considerable uncertainty around this cut‐off distance (95% limits: 13–149 km). The results support a link between Atlantic salmon farms and sea lice burdens on sea trout in the west of Scotland and provide the type of information required for marine spatial planning.     

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.     

Diet,size and location as determinants of n‐3 long‐chain polyunsaturated fatty acid content in farmed Atlantic Salmon (Salmo salar)

We explored how currently manufactured feeds, under real‐world conditions and across geographically distinct locations, promoted flesh n‐3 long‐chain polyunsaturated fatty acid (LC‐PUFA, i.e. 20:5n‐3 + 22:6n‐3) levels in various life stages of farmed Atlantic Salmon (Salmo salar). Potential effects on flesh LC‐PUFA included: (1) diet and fish weight at one Canadian east coast farm, (2) diet and farm location across six east coast farms, and (3) diet and farm location between east and west coast farms. For objectives 1 and 2, salmon were fed a currently manufactured feed (labelled as feeds A, B or C) and harvested at 1, 3 and 5 kg. LC‐PUFA levels in 5 kg (harvest size) fish were then compared to previously published values for west coast farmed Atlantic Salmon (Obj. 3). Combined results revealed that variability in LC‐PUFA levels was better explained by diet than by fish weight or farm location. Fish size, however, was also important for two reasons. First, feeding a high LC‐PUFA diet early in life appeared important for ensuring high LC‐PUFA levels at harvest size. Second, salmon flesh LC‐PUFA levels increased with fish size, but only when dietary LC‐PUFA was provided above an apparent threshold value (~3000 mg per 100 g or 10% of total fatty acids) that likely promoted LC‐PUFA incorporation and storage. Overall, our comparison makes new recommendations for feed manufacturers and demonstrates that farmed Atlantic Salmon reared under real‐world conditions on currently available salmon feeds were good sources of n‐3 LC‐PUFA to consumers.     

Molecular tracing confirms that infection with infectious pancreatic necrosis virus follows the smolt from hatchery to grow‐out farm

Infectious pancreatic necrosis (IPN) is an important restraint to production of salmonids in aquaculture globally. In order to implement efficacious mitigation strategies for control of this disease, it is important to understand infection routes under current production systems. IPN virus has been shown to be transmitted vertically in Rainbow trout, from broodstock to fingerlings in hatcheries, and there is circumstantial evidence suggesting that vertical transmission can also occur in Atlantic salmon, in addition to horizontal transmission between grow‐out fish in farms. In this study, we show that the smolt carries infection with IPN from hatchery to the marine farm. We do this by comparing sequences from fish groups taken both in hatcheries and on corresponding marine grow‐out farms. We use statistical analysis to prove that sequences obtained from the same fish group in both hatchery and marine farm are more similar than sequences obtained from random fish groups on hatcheries and marine farms.     

Genetic analysis of Atlantic salmon captured in a netting station reveals multiple escapement events from commercial fish farms

Microsatellite DNA analysis and statistical assignment methods were implemented to identify the origin of 190 farmed escaped Atlantic salmon recaptured over a period of 2 months at a netting station located in Trondheim fjord, Norway. Samples were also collected from farms within the region. The escapees originated from a minimum of two sources, separated in time of capture at the netting station. The majority of the escapees captured in the early period probably originated from a single farm within the region, while escapees captured in later period probably originated from multiple farms, including from outside of the region. Biological data from the escapees supported these conclusions. This study serves to exemplify the use of genetic methods to assist fisheries management.     

Prevalence,geographic distribution and phenotypic differences of Piscirickettsia salmonis EM‐90‐like isolates

Early reports accounted for two main genotypes of Piscirickettsia salmonis, a fish pathogen and causative agent of piscirickettsiosis, placing the single isolate EM‐90 apart from the prototypic LF‐89 and related isolates. In this study, we provide evidence that, contrary to what has been supposed, the EM‐90‐like isolates are highly prevalent and disseminated across Chilean marine farms. Molecular analysis of 507 P. salmonis field isolates derived from main rearing areas, diverse hosts and collected over 6 years, revealed that nearly 50% of the entire collection were indeed typed as EM‐90‐like. Interestingly, these isolates showed a marked host preference, being recovered exclusively from Atlantic salmon (Salmo salar) samples. Although both strains produce undistinguishable pathological outcomes, differences regarding growth kinetics and susceptibility to the antibiotics and bactericidal action of serum could be identified. In sum, our results allow to conclude that the EM‐90‐like isolates represent an epidemiologically relevant group in the current situation of piscirickettsiosis. Based on the consistency between genotype and phenotype exhibited by this strain, we point out the need for genotypic studies that may be as important for the Chilean salmon industry as the continuous surveillance of antimicrobial susceptibility patterns.     

Assessing the influence of gilthead sea bream escapees in landings of Mediterranean fisheries through a scale‐based methodology

Gilthead sea bream (Sparus aurata L.) aquaculture has rapidly spread around the Mediterranean Sea. Fish escapes from sea cages are one of the major problems for the industry and also represent a threat to the marine environment. Fishery catches are also influenced by escape events, being mirrored in increased landings of cultured species. However, within the Mediterranean, studies shedding light on the incidence of escaped individuals in fisheries landings are scarce. Firstly, the present study describes a simple scale‐examination methodology to distinguish escaped from wild S. aurata landed by coastal fisheries. Secondarily, the incidence of escapees is assessed within landings of the species in the western Mediterranean. The scale readings revealed a monthly incidence of escapees between 11.2 and 20.8%, representing 6.8% of the total income derived from these landings. Moreover, morphological differences between wild fish captured near and far from fish farms point towards escape events as a source of potential genetic admixture between cultured and wild genotypes. Socio‐economic and ecological implications of escapees are discussed, and a set of management guidelines proposed, to prevent and/or mitigate the negative influences of escaped fish on the ecosystem and traditional users of the coast such as fisheries.     

Investigation of co‐infections with pathogens associated with gill disease in Atlantic salmon during an amoebic gill disease outbreak

Gill diseases are a complex and multifactorial challenge for marine farmed Atlantic salmon. Co‐infections with putative pathogens are common on farms; however, there is a lack of knowledge in relation to the potential effect co‐infections may have on pathology. The objective of this study was to determine the prevalence and potential effects of Neoparamoeba perurans, Desmozoon lepeophtherii, Candidatus Branchiomonas cysticola, Tenacibaculum maritimum and salmon gill poxvirus (SGPV) during a longitudinal study on a marine Atlantic salmon farm. Real‐time PCR was used to determine the presence and sequential infection patterns of these pathogens on gill samples collected from stocking until harvest. A number of multilevel models were used to determine the effect of these putative pathogens on gill health (measured as gill histopathology score), while adjusting for the effect of water temperature and time since the last freshwater treatment. Results indicate that between 12 and 16 weeks post‐seawater transfer (wpst), colonization of the gills by all pathogens had commenced and by week 16 of marine production each of the pathogens had been detected. D. lepeophtherii and Candidatus B. cysticola were by far the most prevalent of the potential pathogens detected during this study. Detections of T. maritimum were found to be significantly correlated with temperature showing distinct seasonality. Salmon gill poxvirus was found to be highly sporadic and detected in the first sampling point, suggesting a carryover from the freshwater stage of production. Finally, the model results indicated no clear effect between any of the pathogens. Additionally, the models showed that the only variable which had a consistent effect on the histology score was N. perurans.     

The environmental and host‐associated bacterial microbiota of Arctic seawater‐farmed Atlantic salmon with ulcerative disorders

The Norwegian aquaculture of Atlantic salmon (Salmo salar L.) is hampered by ulcerative disorders associated with bacterial infections. Chronic ulceration may provide microenvironments that disturb the normal microbial biodiversity of external surfaces. Studying the composition of microbial communities in skin ulcers will enhance our understanding of ulcer aetiology. To achieve this, we tested marine farmed Atlantic salmon and sampled the base and edge of ulcers at the end of winter (April) and end of summer (September), in addition to skin mucus of healthy individuals. In order to assess microbiota associated with the host and obtain insight into the environmental ecology, we also sampled sea water, the sediment layer underneath the farm facility and the distal intestine of Atlantic salmon. The skin microbiota of Atlantic salmon was different from that of the surrounding water. Residential Tenacibaculum and Arcobacter species persistently dominated the cutaneous skin and ulcer mucus surfaces of Atlantic salmon during both winter and summer periods. The intestinal microbiota was dominated by Mycoplasma with an increase in Aliivibrio and Alcaligenes abundance in the intestine of fish with ulcerative disorder at the end of winter. These findings suggest the presence of resilient microbes in the mucus surfaces of Atlantic salmon.     

Evaluation of sea lice abundance levels on farmed Atlantic salmon (Salmo salar L.) located in the Broughton Archipelago of British Columbia from 2003 to 2005

Salmon farming began in British Columbia (BC) in the 1970s and in 2006, aquaculture represented BC's largest agricultural export. Along with this growth in production has been a growth in controversy, including the concern that sea lice originating from Atlantic salmon farms negatively impact wild juvenile pink salmon in the Broughton Archipelago. To understand the dynamic interaction between wild and farmed fish, data for on‐farm abundance of sea lice are required. In this study, 33 000 Atlantic salmon from 20 active farms were examined over 3 years. Two species of lice were found: Lepeophtheirus salmonis and Caligus clemensi. Inter‐annual and seasonal variations in abundance levels occurred with lower levels of L. salmonis in 2003 compared with 2004 and 2005, while C. clemensi levels were highest in 2003. The abundance of L. salmonis was greater on older farmed fish. The findings are compared with European and eastern Canadian sea lice reports, and possible sources of sea lice on farmed salmon are discussed.     

A survey of salmon gill poxvirus (SGPV) in wild salmonids in Norway

In 2016, the Norwegian health monitoring programme for wild salmonids conducted a real‐time PCR‐based screening for salmon gill poxvirus (SGPV) in anadromous Arctic char (Salvelinus alpinus L.), anadromous and non‐anadromous Atlantic salmon (Salmo salar L.) and trout (Salmo trutta L.). SGPV was widely distributed in wild Atlantic salmon returning from marine migration. In addition, characteristic gill lesions, including apoptosis, were detected in this species. A low amount of SGPV DNA, as indicated by high Ct‐values, was detected in anadromous trout, but only in fish cohabiting with SGPV‐positive salmon. SGPV was not detected in trout and salmon from non‐anadromous water courses, and thus seems to be primarily linked to the marine environment. This could indicate that trout are not a natural host for the virus. SGPV was not detected in Arctic char but, due to a low sample size, these results are inconclusive. The use of freshwater from anadromous water sources may constitute a risk of introducing SGPV to aquaculture facilities. Moreover, SGPV‐infected Atlantic salmon farms will hold considerable potential for virus propagation and spillback to wild populations. This interaction should therefore be further investigated.     

Atlantic salmon in the North Pacific

The first catches of Atlantic salmon, Salmo salar L., in British Columbia (BC) waters occurred in 1987. The first reported escape of Atlantic salmon (2000 individuals) occurred in 1988. From 1988 to 1995, 97 799 Atlantic salmon were reported escaped from net pens in BC but the true number was higher as not all escapes are reported. Since 1987 a total of 9096 Atlantic salmon was caught in the coastal marine waters of BC, Washington and Alaska, and 188 were caught in fresh water. Most catches occurred in the Johnstone Strait area, where the abundance of salmon farms is highest. The most distant recovery occurred in 1994 when an Atlantic salmon was caught near the western end of the Alaska Peninsula. There have been no reports of successful reproduction of Atlantic salmon in the wild and no feral juveniles have been found. Atlantic salmon caught in the ocean in BC have substantial amounts of adipose tissue and they are heavier at length than fish caught in Alaska. The proportion of fish with prey items in their stomachs is generally low but higher in Alaska (13.1%) than in BC (5.8%). Most fish caught in fresh water are either maturing or mature.     

Incidence and timing of wild and escaped farmed Atlantic salmon (Salmo salar) in Norwegian rivers inferred from video surveillance monitoring

Run timing of escaped farmed Atlantic salmon Salmo salar vs. wild fish was compared by the use of video camera surveillance in 15 rivers over several years, covering 1600 km of the Norwegian coastline (from 58°N to 69°N). Annual runs of wild salmon varied among rivers from <200 fish to more than 10 000. During the surveillance period that for most rivers extended from late May to early October, larger‐sized salmon (fish ≥ 65 cm) generally entered the rivers earlier than small fish. The percentage of salmon identified as escaped farmed fish ranged from 0.1% to 17% across rivers with an average of 4.3%. Estimates of escapees are, however, assumed to represent minimum values because an unknown number of farmed fish passing the video cameras may have been misclassified as wild fish. By the use of a linear mixed model and generalised additive mixed models, it was found that the relationship between run timing and fish length differed significantly between farmed and wild salmon. While small‐sized farmed and wild fish (<65 cm) entered the river at about the same time, wild large salmon returned on average 1–2 weeks earlier than similarly sized escapees. The proportion of large‐sized farmed escapees also increased until late August and decreased thereafter. In contrast, there was a relatively constant and lower proportion of small‐sized escapees throughout the season. Within the surveillance period, there was no evidence of any exceptionally late runs of fish classified as escaped farmed salmon.     

A survey of wild marine fish identifies a potential origin of an outbreak of viral haemorrhagic septicaemia in wrasse,Labridae, used as cleaner fish on marine Atlantic salmon,Salmo salar L., farms

Viral haemorrhagic septicaemia virus (VHSV) was isolated from five species of wrasse (Labridae) used as biological controls for parasitic sea lice predominantly, Lepeophtheirus salmonis (Krøyer, 1837), on marine Atlantic salmon, Salmo salar L., farms in Shetland. As part of the epidemiological investigation, 1400 wild marine fish were caught and screened in pools of 10 for VHSV using virus isolation. Eleven pools (8%) were confirmed VHSV positive from: grey gurnard, Eutrigla gurnardus L.; Atlantic herring, Clupea harengus L.; Norway pout, Trisopterus esmarkii (Nilsson); plaice, Pleuronectes platessa L.; sprat, Sprattus sprattus L. and whiting, Merlangius merlangus L. The isolation of VHSV from grey gurnard is the first documented report in this species. Nucleic acid sequencing of the partial nucleocapsid (N) and glycoprotein (G) genes was carried out for viral characterization. Sequence analysis confirmed that all wild isolates were genotype III the same as the wrasse and there was a close genetic similarity between the isolates from wild fish and wrasse on the farms. Infection from these local wild marine fish is the most likely source of VHSV isolated from wrasse on the fish farms.     

PCR survey for Paramoeba perurans in fauna,environmental samples and fish associated with marine farming sites for Atlantic salmon (Salmo salar L.)

Amoebic gill disease (AGD) caused by the amoeba Paramoeba perurans is an increasing problem in Atlantic salmon aquaculture. In the present PCR survey, the focus was to identify reservoir species or environmental samples where P. perurans could be present throughout the year, regardless of the infection status in farmed Atlantic salmon. A total of 1200 samples were collected at or in the proximity to farming sites with AGD, or with history of AGD, and analysed for the presence of P. perurans. No results supported biofouling organisms, salmon lice, biofilm or sediment to maintain P. perurans. However, during clinical AGD in Atlantic salmon, the amoeba were detected in several samples, including water, biofilm, plankton, several filter feeders and wild fish. It is likely that some of these samples were positive as a result of the continuous exposure through water. Positive wild fish may contribute to the spread of P. perurans. Cleaner fish tested positive for P. perurans when salmon tested negative, indicating that they may withhold the amoeba longer than salmon. The results demonstrate the high infection pressure produced from an AGD‐afflicted Atlantic salmon population and thus the importance of early intervention to reduce infection pressure and horizontal spread of P. perurans within farms.