There are now many more farmed than wild salmon in the Atlantic. One of the HPRΔ from 2008 emerged again in 2016 (eight years later) while another HPRΔ from 2008 emerged in 2013 (after five years). It was further suggested that ISA emerges in farmed salmon after mutation in HPR0 variants transmitted from wild salmonids, followed by transmission between sites due to movement of salmon, well boat transport and other farming activities. “In Norway, it’s the sacred salmon.”, As Wild Salmon Decline, Norway Pressures Its Giant Fish Farms. Now, at 55, he keeps a lot more of them: around 1.2 million just in one windswept spot off the stunning coast of Norway, a giant farm with six large, circular structures each containing around 200,000 fish. Identical viruses to Scottish and Norwegians HPR0 viruses are present in Chile. Salmon and trout were also collected in the sea using fish traps in the fjords; Agdenes, Kvaløya, Namsfjorden and Altafjorden (Fig 1). Data curation, Writing – original draft, Much of Norwegian salmon is farmed. The wild salmon from grocery stores was either fresh or previously frozen, and in restaurants—which ranged from high-end establishments to take-out sushi joints—it was part of a … This lead to a new situation in 1994 with only a single outbreak of ISA . This ancestor was the source of virus that since then evolved into 3 lineages that all contain recent isolates (2014 or younger). Subclade CIIc contains both HPR0 and HPRΔ ISA viruses collected from salmon in the Faeroe Islands, while subclade CIId contains HPR0 ISA viruses from farmed salmon in Faeroe Islands and Finnmark county, and one HPR0 variant (NT242/16) from wild salmon in Trøndelag (Fig 4). Four fragments covering the full length of segment six, were amplified by nested PCR using the Roche Expand HiFi PCR System (Roche, 4738276001) with one overlapping and one unique primer in the first and second reactions. This clade also includes ISAV (H97/04, MR104/05, Scot157/08) from three different brood fish locations (fresh water), two in Norway and one in Scotland. The infectious salmon anaemia virus (ISAV) is an important pathogen on farmed salmon in Europe. e0215478. The tree was colored according to the most likely country where nodes have existed. The high identity between the wild and farmed ISA viruses in CII suggests recent transmissions. Including virulent variants in the analysis show that they belong in the same four clades supporting the hypothesis that there is a high frequency of transition from low to high virulent variants in farmed populations of salmon. Disease – the farmed population of Atlantic salmon vastly outnumbers wild salmon. This study show that all known ISA viruses, HPR0 and HPRΔ, of European origin group into four major clades where members of three of these are present in Norwegian farmed salmon. Subclade, CIIIa, includes 43 ISA viruses collected in the period 2008–2017 from six different counties in Norway in addition to the two viruses from Russia (Fig 4). Long, bright summer nights make it possible to go fishing late at night or early … In the period (1993–2018) after this new management there has been an average of 10 outbreaks each year ranging from one (1994 and 2011) to 23 (2000). . The ISAV (N = 28) in clade III (CIII), collected in the period 2005–2014, consists exclusively of low virulent ISA viruses from farmed Norwegian salmon (Fig 2). Wild salmonids (Salmo salar and S. trutta) were collected in rivers in western Norway (Rogaland–Møre og Romsdal), in the sea (Agdenes, Kvaløya, Namsfjorden) and rivers (Orkla, Gaula, Stjørdalselva, Steinkjærelva, Namsen) in Trøndelag, and in Altafjorden (sea) and Altaelva (river) in Finnmark. It must also be added that viruses with similar HPRΔ have been found the same year as far apart as Sør-Trøndelag (ST77/03) and Troms (T2003/03A) counties suggesting separate mutation events and not horizontal transmission (Figs 1 and 6). Among the remaining ISAV in CIV there are seven sequences from brood fish locations in fresh water, MR104/05 and H97/04—H97f/04. HPR0 sequences from wild fish in Norway are limited to Clades I and II, where relatively recent jumps between farmed and wild hosts are indicated in Clade II. It looks good, but I don’t know,” Mr. Sandven said, when asked if it might have farmed salmon genes. Within CIV there are eight subclades with support values above 70.0%. SKJERJEHAMN, Norway — As a teenager, Ola Braanaas kept a few fish in an aquarium in his bedroom. Presence of HPR0 viruses at smolt production sites and the importance of these viruses as a source for the virulent ISA virus strains (HPRΔ) was further supported by studies published in 2012 [53, 55]. Discover a faster, simpler path to publishing in a high-quality journal. The study showed that ISA viruses from different areas along the Norwegian coast were closely related and that this relationship reflected the origin of the eggs from which the salmon were hatched. ISA viruses were first detected in wild trout and salmon at several locations in Scotland [38, 39] and later in the same two species collected in Norway [37, 40]. It has already been thoroughly documented that HPR0 viruses can be found in brood fish, in fresh water production, and in salmon at marine sites [48, 53, 55]. The ISAV found in wild salmon in Trøndelag have not been seen in farmed salmon in this area giving little support to an assumed transmission between wild and farmed salmon, while nearly identical ISAV have been found in farmed and wild salmon in Finnmark (Fig 4). These predators eat the young wild salmon in greater numbers than normal as they make their way out to sea, or sometimes even force them into the farm cages. I live in South Africa and the type of salmon common here is Norwegian- is it wild caught or farm raised? The specific roles of the authors are articulated in the author contributions section. These viruses group into four distinct clades (CI–CIV). here. The scale bar shows the number of nucleotide substitutions as a proportion of branch lengths. The HPR0 viruses from farmed Norwegian salmon in CII have been found in sea water only. The relatively low correlation between genetic distance and sampling time (r2 = 0.08 with Clade I included and 0.26 without Clade I) suggested a high degree of rate variation between branches. But so divisive is the debate that environmental groups do not trust statistics provided by the farmers, and the two sides don’t agree on the facts. The wild Norwegian salmon are members of an ancient species that, early in its life cycle, heads down river, swimming through Norway’s famous fjords, and out to saltwater feeding grounds, before returning to their native rivers to spawn. Salmon in a hatchery in Byrknesoy, from where they are later sent to a processing factory. The three other clades (II, III and IV) share a common ancestor that may have existed approximately around the time when modern salmonid farming began, although the estimate has a wide uncertainty interval (best estimate: 1966 with 95% HPD interval 1934–1987). Divergence of Clade I from the other sequences was estimated to have occurred around the year 1941 (95% HPD interval: 1884–1976). The high numbers of different HPRΔ variants found every year in Norway suggest that such transitions are of major importance for the yearly outbreaks of ISA in Norway. Salmon flesh is generally orange to red, although white-fleshed wild salmon with white-black skin colour occurs. You would have to check the labels or with your fishmonger to confirm though. The best-fitting nucleotide substitution model was used during maximum likelihood analysis and the tree was bootstrapped (50 000 quartet puzzling steps) in TREE_PUZZLE. They are therefore not epidemiologically linked, and have probably evolved as separate lineages at least since the early days of industrialization of salmon farming in Europe (estimate for MRCA: 1966 (1934–1987)). No, Is the Subject Area "Islands" applicable to this article? All current sequence diversity within each of these three clades has likely evolved after the beginning of modern aquaculture in Europe, with estimates on node ages of 1997 (95% HPD interval: 1985–2004) for Clade III, 1987 (95% HPD interval: 1974–1997) for Clade IV and 1993 (95% HPD interval: 1977–2003) for Clade II (Fig 3). H112a/04 represents a completely different HPRΔ compared to the other members of CIIb. The annual loss of wild salmon to Norwegian rivers due to salmon lice was estimated at 50 000 adult salmon for the years 2010-2014. In Norway, wild salmon are known to pick up sea lice when they swim from the sea to the fjord in spring to spawn in the rivers, but the lice usually fall off during the river migration. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. The majority of the salmon (N = 436) from Western Norway were collected as brood fish from hatcheries for restocking of wild salmon in the period 2009–2013, while the trout (N = 253) were collected by electro-fishing in rivers and by net in the fjords. These studies show that there are limited numbers of ISA viruses circulating in Norwegian salmon production. No, Is the Subject Area "Viral transmission and infection" applicable to this article? These viruses represent, most likely, nine or more separate mutations from HPR0 viruses. The CI viruses from wild salmon in Norway (2013–2015) are only distantly related to those from farmed salmon in the Faeroes and give no indication of recent transmission between wild salmon and farmed salmon or vice versa. Phylogenetic analyses of the surface protein hemagglutinin-esterase gene from nearly all available ISAV from Norway, Faeroe Islands, Scotland, Chile and wild salmonids in Norway show that they group into four major clades. Tips in the tree were assumed to provide equal amount of information on the probability of the shared node location. A total of 21 segment six sequences were obtained from wild salmonids in Norway (S1 Table). An alignment containing all available European ISAV HPR0 (N = 109) sequences covering the near full-length segment 6 (HE gene) was first imported into Mega6  where a phylogenetic tree was obtained by Maximum likelihood under the General Time Reversible model  for nucleotide substitution, together with a discrete gamma model of rate heterogeneity amongst sites (GTR+G). Phylogenetic analysis of segment six sequences (N = 118) from the low virulent (HPR0) ISA viruses grouped them into four major, supported, clades (C) named: CI, CII, CIII and CIV (Fig 2). Low-virulent HPR0 ISA virus sequences have been obtained from all counties with commercial salmon farming in Norway, while ISA virus sequences from wild salmonids have only been obtained from the counties Rogaland, Sør Trøndelag, Nord Trøndelag and Finnmark (Fig 1). Then, the rod strained, and he slowly reeled in a small, shiny, olive brown salmon weighing a couple of pounds. The aim of the present study was to provide new knowledge about ISA viruses in wild salmonids along the Norwegian coast, the possible impact of transmission of ISA viruses from farmed to wild salmonids, and wild salmonids as possible biological vectors for ISA viruses. estimated 50,000 adult wild fish a year in Norway’s rivers. Inge Sandven, right, the head of the Dale Hunters’ and Anglers’ Club, by the Dale River outside Bergen, Norway. Resources, The best fitting root for the tree was identified through regression, and a weak temporal structure (r2 = 0.08) was evident. So depleted are stocks of wild salmon that around 100 of Norway’s 450 salmon rivers are closed to anglers. 4% salt solution injected to enhance flavor. Blackwing Meats | Wild Norwegian Portioned Salmon (1lb. Other priors were left as the default setting in beast. This clade represents a group of viruses that seems to be maintained and circulated in populations of farmed Norwegian salmon with no indication of transmission to wild salmonids. Considering the fact that the dominating ISA viruses in the Norwegian salmon farming industry belong to clade CIII and CIV, and not to the two clades where the majority known viruses from Norwegian wild salmon can be found, suggest that the viruses causing the majority of the ISA outbreaks in Norway are maintained or circulated in farmed salmon. Writing – review & editing, Roles The other three clades, CII–CIV, of HPR0 ISAV all include viruses from farmed salmon in Norway. ISA virus Scot157/08 is from a brood fish location in Scotland. The three ISA viruses collected in Norway in 1996–1998 are distinctly different from the remaining ISA viruses collected 10 years later from Scotland and Chile. Alignment of the putative amino acid sequences shows that this group contains four HPRΔ variants, where the first is present in 1993 and 2003, the second in 2002, 2003, 2004 and 2005, the third in 2004, and the fourth in 2007. This suggests that the evolution of HPR0 viruses is clocklike only to a limited degree, and that branches in the tree evolve with variable rates on the time-scale that we have analyzed. Several cases where HPR0 and HPRΔ ISA viruses are identical in the phylogenetic analysis, based on 947 nt from the region coding the surface domain of the HE protein, suggest a recent transmission from low to high virulent variants (Figs 4 and 6). The impacts of escaping farmed salmon on wild salmon populations are a high concern, as are the impacts of parasitic sea lice on wild salmon and particularly sea trout. The CII-viruses from farmed salmon in Norway are closely related to viruses from wild salmon from both Finnmark and Trøndelag, and one virus, FO/01/08, from the Faeroes is identical to three viruses (NT197/15, NT205/15, FM200b/16) from wild salmon in Norway. The viruses in this clade have been collected in six different counties (from Hordaland to Troms), and in the viruses collected in the period 1996–2005 six different HPR including HPR0 are present. It also created 61,000 jobs. The fish farmers argue that they play a vital role in feeding the planet, and that they produce a crop worth $8 billion annually to Norway, accounting for about 8 percent of the country’s exports. The prevalence of ISA virus in wild salmon (Salmo salar) and trout (Salmo trutta) in western Norway was low, 0.5% (2/436) and 1.6% (4/253), respectively. ISAV from farmed salmon in Norway (Black), Faeroe Islands (Green), Scotland (Blue), Chile (Orange), and wild salmonids in Norway (Red). We set high standards and our model of sustainably managed aquaculture is recognised worldwide. These HPRΔ sequences provide 10 different HPR variants which means that they represent a minimum of 10 different new mutations events, ie. Nutrition Facts: Calories: 288 | Protein: 36g | Carbs: 0g | Fat: 15g Based on 6oz. Canadian and Scottish salmon were also tested. University of Bergen, Fish Diseases Research Group, Bergen, Norway, Roles However, including all ISA virus sequences (N = 76, S1 Table) collected from the 21 salmon production sites in Troms County that experienced ISA outbreaks in the period 2007–2009, provide seven different HPRΔ variants which show that, in addition to horizontal transmission, there is also a number of unique mutations suggesting several primary outbreaks in the area in this period. No, Is the Subject Area "Marine fish" applicable to this article? The HPR0 viruses that are related to these HPRΔ variants have only been found in farmed salmon and are most likely a result of a combination of vertical transmission and horizontal transmission within populations. Supervision, However, an even higher prevalence of ISAV was registered in trout (S. trutta) from rivers in Sogn og Fjordane County in 2001–2002 during outbreaks of ISA in salmon farms in the area . The scale bar shows the number of nucleotide substitutions as a proportion of branch lengths. This segment has been used in several earlier studies of the relationship between existing ISA viruses and for inferring short and long distance transmission [33, 34, 37, 41, 43, 46, 48, 49, 51, 52, 53, 55, 58, 70, 71, 72]. The shape parameter of the gamma distribution and ratio of transition rate to transversion rate were estimated from the data. It was shown in 1987  that ISA was a transmissible disease and this study was followed by several transmission experiments all resulting in high mortalities in the challenged groups of salmon [2, 5, 6, 7, 8, 9, 10, 11, 12, 13]. Salmon infected with ISAV escaped from a farm in this area early in the epizootic and this could have contributed to what seems to be a massive horizontal transmission of the virus resulting in a high number of outbreaks (Fig 5). https://doi.org/10.1371/journal.pone.0215478.g003. Based on these results we recommend that, due to a high occurrence of mutations of HPR0 variants resulting in HPRΔ viruses that cause outbreaks of ISA, a shift from focusing only on HPRΔ variants and outbreaks of ISA is needed. It should be noted that ISA was not diagnosed in the brood fish population, and it is not known if the HPRΔ variant could cause disease in salmon. Get the facts about farm-raised salmon from Norway. Our cooperation with M. Karlsen does not alter our adherence to PLOS ONE policies on sharing data and materials. Evidence of vertical transmission has been presented, but there is still an ongoing discussion of the importance of circulation of ISAV via salmon brood fish. Equally important is the protection of wild salmonids from virulent ISAV produced in farmed salmon. This clade contains a number of HPR0 ISA viruses from Norway including viruses from two different brood fish locations in addition to a HPR0 variant from a Scottish brood fish population. Five different HPRs, including HPR0, were present in the farmed salmon (N = 10) in 2008, while two HPRΔ and one HPR0 (N = 7) were present in 2014. No, Is the Subject Area "Norway" applicable to this article? The natural colour of salmon results from carotenoid pigments, largely astaxanthin, but also canthaxanthin, in the flesh. Subclade CIIb contains eight viruses collected in the period 2000–2004 from salmon in three counties in western Norway (Fig 4). Data Availability: All relevant data are within the manuscript and its Supporting Information files. The analyses of our data give support this conclusion, but the situation was more complex, and the hypothesis suggesting an epizootic resulting from a primary outbreak does not give the complete picture of what happened in this area. The disease, infectious salmon anaemia (ISA), was officially discovered in 1984 among salmon parr in a hatchery in Western Norway . The latter scenario would be expected to result in viruses from wild hosts distributed more equally to all clades. Kurt Oddekalv, leader of the Green Warriors of Norway, says the system is a sign of “panic from the Fisheries Ministry.”. Conceptualization, Clade CIV provides undisputable evidence of long distance transmission of HPR0 ISA viruses from Europe (Norway and Scotland) to Chile. Although it can’t be excluded that wild fish infected with HPR0 ISAV belonging to Clades III and IV exist (undetected by us due to sampling bias), an alternative explanation to the lack of wild sources of viruses in these clades is that they are almost exclusively circulating in farmed populations. Mr. Sandven knows this because he supervises a wild salmon hatchery, and takes DNA samples from fish caught in this river before they are used for breeding. Visualization, This is the first study of European ISA viruses from farmed Atlantic salmon (Salmo salar) that includes the majority of available segment six sequences in addition to 21 ISA viruses from wild salmon (Salmo salar) and trout (S. trutta) in Norway. The viruses have been obtained from farmed salmon in both fresh and sea water. Clade II (CII) consists of several HPR0 ISA viruses (N = 26) collected from wild and farmed salmon in Norway and farmed salmon in the Faeroe Islands collected in the period 2006–2018 (S1 Table and Fig 2). Mr. Braanaas, the owner of Firda Seafood, says that there are already rules in place to control the lice, and that he will go to court if he is ordered to reduce production because of problems from other farms in his region. In just 15 minutes at one river pool, set against a spectacular backdrop of tree-covered hills, he had three bites but no catches. Atlantic salmon are, well, native to the … The densities of ISA virus RNA were also low in these samples and it was only possible to sequence segment six from one of the positives (R170/09), a trout collected in a river in Rogaland County (Fig 1 and S1 Table). The four HPRΔ sequences in this clade provide three different HPRs, one from two viruses in Rogaland (2017) and two others from two viruses (H195/15 and H248/18) from Hordaland. These viruses could have arisen from the same HPR0 in four separate mutation events. The maximum likelihood trees were bootstrapped (50000 puzzling steps) in TREE_PUZZLE. CHILE IS OUR PRIMARY SUPPLIER OF ATLANTIC SALMON. Yes The four HPR0 ISA viruses from wild salmon in Trøndelag constitute two separate subclades within CI. Members of this clade have not been detected in farmed salmon in Norway. Once a rarity on global dinner tables, salmon is a staple today, thanks to a fish farming industry that has expanded at breakneck speed in recent decades, including in Norway, where in 2016 around 1.18 million metric tons were produced. The salmon and trout from rivers in middle Norway (Trøndelag) and river Alta (Finnmark) were collected by fly-fishers, while the salmon and trout in the sea (Agdenes, Kvaløya, Namsfjorden and Altafjorden) were collected from fish traps (“kilenot”) (Fig 1 and Table 1). Ninety-seven percent of the salmon consumed in Sweden is farmed in Norway. The ISA virus segment six nucleotide sequences were assembled with the help of Vector NTI software (InforMax, Inc.). Information on the health of Norway’s farmed fish is now publicly available online. Few people know the fishing grounds of the Dale River as well as Inge Sandven, the head of the Dale Hunters’ and Anglers’ Club. Norway is the biggest producer of farmed salmon in the world, with more than one million tonnes produced each year. The Ct values obtained for the elongation factor α, that was used as a control for the quality of the RNA extractions, ranged from 14.4 to 18.0 in the screening of the gill samples from the wild salmonids. However, as already published, stress or maturing of salmon infected with HPR0 ISA virus seem to cause an increase in virus replication increasing the chances for mutations to occur [15, 16]. 2011, 2012]. Norway’s biggest producer, Marine Harvest, is also unhappy with the new protocol, which it describes as premature, and wants more work done on the methodology used to decide when there is a lice problem that needs to be addressed. Mercury and … Ola Braanaas, the company’s owner, said he would go to court if he were ordered to reduce production because of problems from other farms in his region. Time and geographical occurrence suggests that they represent a minimum of 10 % was used for sequencing HPR0 ISA.... Date, and tree tips represent the MRCAs of each sequence Salmo salar.. Ethics committee ( 2.7.1 ) Faeroes [ 58 ] sampling dates and available year... Represented two different HPRΔ compared to the … salmon is now a global.... On vertical transmission via embryos from Europe ( Norway and 11 from the data branches was employed following. 41.7 % of the four HPR0 ISA viruses detected during the first outbreaks of ISA collected! 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