The economic impact of decreased mortality and increased growth associated with preventing, replacing or improving current methods for delousing farmed Atlantic salmon in Norway.

Impacts of salmon lice is a major concern for a sustainable production of farmed Atlantic salmon in Norway. Most treatment methods for removal of salmon lice have associated increased mortality and decreased growth in a period after delousing, which affects the profitability of the farmer, and causes poor welfare and sustainability. In addition, the variance in mortality and growth, especially after non-medicinal treatment methods, is high, which makes it hard for a farmer to decide which control measure to apply to keep lice levels below the legal limit. In this study, we have applied a stochastic partial budget approach to assess the economic impact of reducing mortality and increasing growth of farmed Atlantic salmon by preventing, replacing and improving current delousing methods in Norway. We have simulated a production cycle of two different smolt-groups to find the outcome (harvested biomass, average end weight of the salmon, number of dead fish and feed consumption) of production cycles without or with two, three or four delousing treatments in the on-growing phase at sea. The results suggest that accounting for the biological losses associated with lice treatments is important when making choices of delousing strategies. The biological costs of increased mortality and decreased growth associated with especially non-medicinal treatments are expected to be high, but varies substantially. Therefore, the economic benefit of preventing or improving can also be high. The calculations imply that salmon producers could invest a considerable amount in measures for prevention or improvement of thermal treatments before break-even. For example could a farmer use on average 535,313 €/cage/ 1-yearling production in measure to prevent four thermal treatments before it is no longer economical beneficial. Depending on the performance of the four thermal treatments a farmer could use from 319,196-737,934 €/cage/ 1-yearling production on measures of improvement. Replacing one thermal treatment with another immediate treatment method has a minor economic benefit. The results further shows that sales value and feed consumption constitutes the largest share of the change in profit between different treatment regimes. The results from this study also show that not taking into account the risk of mortality and reduced growth associated with the different treatment methods of delousing, could lead to underestimating the benefit of improving, preventing and replacing treatments.

Simulated effects of increasing salmonid production on sea lice populations in Norway.

Norway produces more than one million tonnes of salmonids every year, almost exclusively in open-water net pens. In 2014, the Norwegian government announced plans to increase salmonid production. However, increasing the number of farmed salmonids can have negative effects on the marine environment that threaten the industry's sustainability. In particular, production growth can lead to an increase in density-dependent diseases, including parasitic sea lice. The aim of this study was to simulate the effects of increased salmonid production on sea lice abundance using different scenarios for increasing the number of fish and for the management of sea lice. We used a previously developed, partly stage-structured model based on Norwegian production and environmental data to simulate the different scenarios. Our results show that increasing the marine farmed salmonid population at a national level by two or five times the current production leads to an increase in the sea lice abundance by 3.5% and 7.1%, respectively. We also found that by lowering the maximum allowable level of sea lice to an average of 0.049 adult females per fish, weekly treatments can be used to control sea lice population growth with a five times increase in production. However, this increases the number of farms treating per week by as much as 281.3%, which can lead to high costs and increased mortality among farmed salmonids. Overall, the results from our study shed light on the effects of increasing salmonid production in Norway with respect to the ongoing threat of sea lice infestations.

Realtime case study simulations of transmission of Pancreas Disease (PD) in Norwegian salmonid farming for disease control purposes.

Pancreas Disease (PD) is a viral disease caused by Salmonid Alphavirus (SAV). It affects farmed salmonids in the North Atlantic, and leads to reduced feed intake and increased mortality with reduced production and welfare as a consequence. In 2013, the estimated cost of an outbreak on an average salmon farm was about 6.6 mil €. In Norway, PD has been notifiable since 2008, and regulations to mitigate disease spread are in place. However, despite the regulations, 140-170 farms are affected by PD every year. The aquaculture industry is growing continuously, introducing farms in new geographical areas, and fish are moved between hydrographically separated zones for trade and slaughter. All such movements and relocations need to be approved by the competent authorities. Thus, there is a demand for support to farmers and competent authorities when making decisions on disease management and especially on the effect of moving infected fish. We have used a disease-transmission model for outbreak-simulation in real time for assessing the probability of disease transmission from a farm that gets infected with PD. We have also simulated the effects of three different control-regimes: no stamping-out, delayed stamping-out or immediate stamping-out, on the transmission of PD to surrounding farms. Simulations showed that the immediate stamping out of an infected farm led to effective containment of an outbreak. No stamping out led to up to 32.1% of farms within 100 km of the index farm to become effected. We have used real production data for the model building and the scenario simulations, and the results illustrate that a risk assessment of horizontal disease transmission must be undertaken on a case-by-case basis, because the time and place of the outbreak has a large influence on the risk of transmission.

Factors associated with baseline mortality in Norwegian Atlantic salmon farming.

In 2019, it was estimated that more than 50 million captive Atlantic salmon in Norway died in the final stage of their production in marine cages. This mortality represents a significant economic loss for producers and a need to improve welfare for farmed salmon. Single adverse events, such as algal blooms or infectious disease outbreaks, can explain mass mortality in salmon cages. However, little is known about the production, health, or environmental factors that contribute to their baseline mortality during the sea phase. Here we conducted a retrospective study including 1627 Atlantic salmon cohorts put to sea in 2014-2019. We found that sea lice treatments were associated with Atlantic salmon mortality. In particular, the trend towards non-medicinal sea lice treatments, including thermal delousing, increases Atlantic salmon mortality in the same month the treatment is applied. There were differences in mortality among production zones. Stocking month and weight were other important factors, with the lowest mortality in smaller salmon stocked in August-October. Sea surface temperature and salinity also influenced Atlantic salmon mortality. Knowledge of what affects baseline mortality in Norwegian aquaculture can be used as part of syndromic surveillance and to inform salmon producers on farming practices that can reduce mortality.

Estimating cage-level mortality distributions following different delousing treatments of Atlantic salmon (salmo salar) in Norway.

This retrospective descriptive study estimates cage-level mortality distributions after six immediate delousing methods: thermal, mechanical, hydrogen peroxide, medicinal, freshwater and combination of medicinal treatments. We investigated mortality patterns associated with 4 644 delousing treatment of 1 837 cohorts of farmed Atlantic salmon (Salmo salar) stocked in sea along the Norwegian coast between 2014 and 2017. The mortality is expressed as mortality rates. We found distributions of delta mortality rate within 1, 7 and 14 days after all six delousing treatments, using mortality rate within 7 days before treatments as baseline. The results show that we can expect increased mortality rates after all six delousing methods. The median delta mortality rates after thermal and mechanical delousing are 5.4 and 6.3 times higher than medicinal treatment, respectively, for the 2017 year-class. There is a reduction in the delta median mortality for thermal and freshwater delousing from 2015 to 2019. There is a wide variability in the mortality rates, in particular for thermal delousing. Our results suggest that the variability in delta mortality for thermal delousing has been reduced from the 2014 to 2017 year-class, indicating an improvement of the technique. However, a significant increase in the number of thermal treatments from 14 in 2015 to 738 in 2018 probably contributes to the overall increased mortality in Norwegian salmon farming.

Spatio-temporal variations in mortality during the seawater production phase of Atlantic salmon (Salmo salar) in Norway.

In a sustainable production of animals, monitoring and minimizing mortality must be a top priority. Systematic measuring of mortality over time can be used to evaluate the impact of changes in management and production strategies in Norway. To aid understanding of the potential for reducing mortality, we have used data from 2014 to 2018 to investigate the spatio-temporal patterns of mortality, by descriptive analyses and statistical modelling of possible determinants of mortality. The results show large differences in mortality across different production zones and between years. The areas with the highest density of farmed salmon are also the ones with highest mortality. The total cumulated mortality of farmed salmon increased from 32.3 million in 2014 to 35.2 million in 2018, corresponding to 14.3% and 15.8% of the standing stock. An initial higher mortality was observed during the first 3 months after stocking (mean: 1.5% [0.9%-8.6%] mortality/month). This was followed by a period of stability and lower mortality (mean: 0.8% [0.9%-3.1%] mortality/month), until month 10, when mortality started to increase again. The month of first stocking, the year of slaughter, production zone and number of months at sea were all found to be statistically significant determinants for mortality, with p-values < 1e-15.

Estimating risk factors for the daily risk of developing clinical cardiomyopathy syndrome (CMS) on a fishgroup level.

Cardiomyopathy syndrome (CMS) is a viral disease, causing significant mortality and decreased welfare in farmed salmon in the North Atlantic Ocean. In Norway, it has become the most important disease in animal husbandry, affecting more than 100 farms each year. Control of CMS is based on mitigation of risk factors, since no treatment or vaccine is available. However, little is known about how the disease spreads and develops, thus rendering disease control difficult for farmers and competent authorities. The objective of the present study was to identify risk factors leading to the development of clinical CMS, using data provided from the salmon producers. Daily production data from individual fishgroups in more than 120 salmon farms along the coast of Norway from fish put to sea in 2012-2014 was collected. The data included cause-specific mortalities, which was used to identify outbreaks of CMS and risk factors for disease. A model for describing the daily probability of outbreak of CMS in each fishgroup was developed. The model was run to find the most likely value for each of the parameters, given the observed outbreak data. From the data, we found that fish in the southern region of Norway have a much higher risk of developing CMS than fish in mid and west (parameter estimates (PE) 4.43 (CI: 2.54-7.04) vs. 3.27 and 2.58 (CI: 2.45-4.37 and 2.01-3.57). Further, across all regions, fish put to sea in the late fall develop CMS twice as often as fish put to sea in the early spring (PE 2.18-2.59; CI:1.54-4.6). Previous outbreaks of pancreas disease increased the risk of getting CMS with 3.36 (CI:2.97-3.78) in the west and 1.41 (CI: 1.24-1.63) in the mid regions and decreased the risk with 0.519 (CI: 0.456-0.611) in the south. Previous outbreaks of heart- and skeletal muscle inflammation increased the risk of CMS with 1.56-1.73 (CI:1.34-2.11) in the mid and south regions, and had no effect in the west. In addition, we found that fish groups originating from certain hatcheries had a higher risk of CMS than other fishgroups, independent on which farm they were farmed on. The risk of developing CMS also increased with the number of days at sea. The use of production data in the study gave the possibility to study disease development on a fish group level, and on a daily basis. Thus, the identification of risk factors provides new possibilities for control of disease.

Indications for a vertical transmission pathway of piscine myocarditis virus in Atlantic salmon (Salmo salar L.).

Losses due to cardiomyopathy syndrome (CMS) keep increasing in salmon-producing countries in the North-Atlantic. Recently, Piscine myocarditis virus (PMCV) has been detected in post-smolts shortly after sea-transfer, indicating a possible carry-over from the hatcheries. In addition, there are reports of prevalences of PMCV as high as 70%-90% in certain groups of broodfish, and a recent outbreak of CMS in the Faroe Islands has been linked to the importation of eggs from a CMS-endemic area. Thus, there is a need to investigate whether PMCV can be transmitted vertically from infected broodstock to their progeny. In the present study, samples from eggs, larvae, fingerlings and presmolt originating from PMCV-positive broodstock from two commercial Atlantic salmon producers were tested for PMCV. The prevalence of PMCV in the broodstock was 98% in the hearts, 69% in the roe and 59% in the milt. Piscine myocarditis virus was detected in all stages of the progeny until and including the 40 g stage. Piscine myocarditis virus was also detected in presmolt sampled for tissue tropism. This provides farmers with several options for minimizing the risk of transfer of PMCV from broodstock to progeny, including screening of broodstock and aiming to use only those that are negative for PMCV or have low levels of virus.

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.

Routine clinical inspections in Norwegian marine salmonid sites: A key role in surveillance for freedom from pathogenic viral haemorrhagic septicaemia (VHS).

Since the mid-1980s, clinical inspections of aquaculture sites carried out on a regular basis by authorized veterinarians and fish health biologists (known as fish health services: FHS) have been an essential part of aquatic animal health surveillance in Norway. The aims of the present study were (1) to evaluate the performance of FHS routine clinical inspections for the detection of VHS and (2) to explore the effectiveness of risk-based prioritisation of FHS inspections for demonstrating freedom from VHS in marine salmonid sites in Norway. A stochastic simulation model was developed to estimate site sensitivity (SeS), population sensitivity (SeP), and probability of freedom (PFree). The estimation of SeS takes into consideration the probability that FHS submit samples if a site is infected, the probability that a sample is tested if submitted, the effective probability of infection in fish with clinical signs, laboratory test sensitivity, and the number of tested samples. SeP and PFree were estimated on a monthly basis over a 12 month period for six alternative surveillance scenarios and included the risk factors: region, species, area production density, and biosecurity level. Model results indicate that the current surveillance system, based on routine inspections by the FHS has a high capability for detecting VHS and that there is a high probability of freedom from VHS in Norwegian marine farmed salmonids (PFree >95%). Sensitivity analysis identified the probabilities that samples are submitted and submitted samples are tested, as the most influential input variables. The model provides a supporting tool for evaluation of potential changes in the surveillance strategy, and can be viewed as a platform for similar exotic viral infectious diseases in marine salmonid farming in Norway, if they share similar risk factors.

Risk factors for outbreaks of infectious pancreatic necrosis (IPN) and associated mortality in Norwegian salmonid farming.

Infectious pancreatic necrosis (IPN) has for many years been considered one of the most important restraints to the production of salmonids in European aquaculture. In Norway, the disease is responsible for high losses in post-smolts in the first few weeks after sea transfer. Despite the importance of IPN, there are few epidemiological studies on risk factors and mitigation strategies. In this paper, we present analyses of data from all cohorts put to sea in 2009 to 2012 on Norwegian marine salmonid farms. The data used were obtained from national registers on salmonid production and disease outbreaks. The results showed that the risk of IPN outbreak was higher for spring versus autumn cohorts, Atlantic salmon versus rainbow trout and for cohorts on farms with previous history of IPN. The risk increased with increasing cohort size and infection pressure, whereas increasing temperature and weight at sea transfer decreased the risk. Estimations from a model of cumulative mortality within the first 6 mo after sea transfer showed that mortality in cohorts with IPN increased to approximately 7.2% as compared to a 'baseline' cohort with a mortality of 3.4%. If the cohort had both IPN and pancreas disease (PD), the estimated mortality increased to 12.9%, and cohorts with both IPN, PD and heart and skeletal muscle inflammation (HSMI) had an estimated mortality of 16.6%, when all other significant factors were kept constant (these were cohort type, year, temperature at sea transfer and weight at sea transfer). Our results provide valuable inputs for mitigation strategies and for economic modelling of consequences of disease.

Spatio-temporal risk factors for viral haemorrhagic septicaemia (VHS) in Danish aquaculture.

Viral haemorrhagic septicaemia (VHS) is an economically very important fish disease in the northern hemisphere. When the VHS virus was first isolated in Denmark 50 yr ago, more than 80% of the 800 Danish fish farms were considered to be infected, but vigilant surveillance and eradication programmes led to a drastic reduction in prevalence, and finally, to complete eradication of VHS. Denmark thus obtained official status as an approved VHS-free member state within the European Union in November 2013. Data on outbreaks within the country have been collected since 1970, and here we combined these data with the geographical coordinates of fish farms to identify clusters of high disease prevalence and other risk factors. Our analyses revealed a statistically significant cluster in the southwestern part of the country, which persisted throughout the study period. Being situated within such a cluster was a significant risk factor for VHS. For freshwater rainbow trout farms situated inland, the number of upstream farms was a determining risk factor for VHS, as was distance to the nearest VHS-infected farm and year. Whether the farm used fresh or marine water in production did not have any influence on the risk of VHS, when accounting for whether the farm was situated inside a cluster of high risk. This information can be used when implementing risk-based surveillance programmes.

Risk factors for cardiomyopathy syndrome (CMS) in Norwegian salmon farming.

Cardiomyopathy syndrome (CMS) has been an economically important disease in Norwegian aquaculture since the 1990s. In this study, data on monthly production characteristics and case registrations were combined in a cohort study and supplemented with a questionnaire-based case-control survey on management factors in order to identify risk factors for CMS. The cohort study included cases and controls from 2005 to 2012. From this dataset differences between all cases and controls were analyzed by a mixed effect multivariate logistic regression. From this we found that the probability of CMS increased with increasing time in the sea, infection pressure, and cohort size, and that cohorts which had previously been diagnosed with heart and skeletal muscle inflammation or which were in farms with a history of CMS in previous cohorts had double the odds of developing CMS. The model was then used to calculate the predicted value for each cohort from which additional data were obtained via the questionnaire-based survey and used as offset for calculating the probability of CMS in a semi-univariate analysis of additional risk factors. Finally, the model was used to calculate the probability of developing CMS in 100 different scenarios in which the cohorts were subject to increasingly worse conditions with regards to the risk factors from the dataset. We believe that this exercise is a good way of communicating the findings to farmers, so they can make informed decisions when trying to avoid CMS in their fish cohorts.

Risk-based methods for fish and terrestrial animal disease surveillance.

Over recent years there have been considerable methodological developments in the field of animal disease surveillance. The principles of risk analysis were conceptually applied to surveillance in order to further develop approaches and tools (scenario tree modelling) to design risk-based surveillance (RBS) programmes. In the terrestrial animal context, examples of risk-based surveillance have demonstrated the substantial potential for cost saving, and a similar benefit is expected also for aquatic animals. RBS approaches are currently largely absent for aquatic animal diseases. A major constraint in developing RBS designs in the aquatic context is the lack of published data to assist in the design of RBS: this applies to data on (i) the relative risk of farm sites becoming infected due to the presence or absence of a given risk factor; (ii) the sensitivity of diagnostic tests (specificity is often addressed by follow-up investigation and re-testing and therefore less of a concern); (iii) data on the variability of prevalence of infection for fish within a holding unit, between holding units and at farm level. Another constraint is that some of the most basic data for planning surveillance are missing, e.g. data on farm location and animal movements. In Europe, registration or authorisation of fish farms has only recently become a requirement under EU Directive 2006/88. Additionally, the definition of the epidemiological unit (at site or area level) in the context of aquaculture is a challenge due to the often high level of connectedness (mainly via water) of aquaculture facilities with the aquatic environment. This paper provides a review of the principles, methods and examples of RBS in terrestrial, farmed and wild animals. It discusses the special challenges associated with surveillance for aquatic animal diseases (e.g. accessibility of animals for inspection and sampling, complexity of rearing systems) and provides an overview of current developments relevant for the design of RBS for fish diseases. Suggestions are provided on how the current constraints to applying RBS to fish diseases can be overcome.

Risk mapping of heart and skeletal muscle inflammation in salmon farming.

Heart and skeletal muscle inflammation (HSMI) is an infectious disease causing losses to the Norwegian salmon farming industry due to increased mortality and high morbidity in infected salmon. The disease is listed as a notifiable disease on list 3 (national list) by the Norwegian Food Safety Authority. HSMI is believed to be a viral disease, but the association to the recently discovered Piscine reovirus (PRV) remains unclear. Undoubtedly, other factors interact to determine whether PRV-infected fish develop disease or not. In this study, logistic regression was used to model the risk of an outbreak of HSMI at the cohort level, by including spatio-temporal risk factors. The data consisted of fish cohorts grown on geo-referenced farms from 2002 to 2010. The risk factors included were: infection pressure, cohort size (maximum number of fish), cohort index (smolt characteristics), cohort lifespan (months in sea) and a geo-index calculated as the position along a local polynomial regression line based on the longitude and latitude of each farm included in the study. The results showed that the risk of developing HSMI increased with increasing cohort lifespan, increasing infection pressure and increasing cohort size, and was mostly low for cohorts grown on farms in Southern-Norway, high for farms in Mid-Norway and variable for farms in Northern-Norway (based on the geo-index). The final model was used to explore three different scenarios with regards to the risk of developing HSMI, and to calculate the probability for each cohort of developing HSMI, independent of their actual disease-status. The model suggested that the probability of developing HSMI was much higher in Mid-Norway than in the rest of the country. Even though PRV seems to be widely distributed in the environment, the finding that infection pressure has a large influence on the probability of developing HSMI, suggests that it might be possible to reduce the number of clinical outbreaks, if measures are taken to reduce infection pressure. However, the prospects of controlling the spread of HSMI and reducing clinical outbreaks might be difficult because of indications of large distance spread of the disease.

Cohort study of effect of vaccination on pancreas disease in Norwegian salmon aquaculture.

Pancreas disease (PD) is an economically important viral disease in Norwegian aquaculture, with 75 to 89 annual outbreaks from 2009 to 2011. To hinder further spread of disease from an initial endemic area on the west coast of Norway, measures for surveillance and control are in place, and the disease is notifiable on a national level. Since 2008, the Norwegian coastline has been divided into 2 administrative zones separated by a production-free area of 10 nautical miles at approximately 63°N. At the same time, a vaccination program involving most marine salmonid farms was initiated by the industry, using a vaccine against PD that was made commercially available in 2007. The effects of the vaccine in the field have been questioned, since the annual number of PD outbreaks has not decreased as expected. However, other production parameters can be used for evaluation of vaccine effect, and in this study the effects of vaccination on cumulative mortality, growth rate, feed conversion factor and number of discarded fish were analyzed using data collected from fish cohorts with and without PD put to sea between spring 2007 and spring 2009. The results show that vaccination against PD has a positive effect in reducing the number of outbreaks, and decreasing cumulative mortality and the number of fish discarded at slaughter.

Quantification of piscine reovirus (PRV) at different stages of Atlantic salmon Salmo salar production.

The newly described piscine reovirus (PRV) appears to be associated with the development of heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon Salmo salar L. PRV seems to be ubiquitous among fish in Norwegian salmon farms, but high viral loads and tissue distribution support a causal relationship between virus and disease. In order to improve understanding of the distribution of PRV in the salmon production line, we quantified PRV by using real-time PCR on heart samples collected at different points in the life cycle from pre-smolts to fish ready for slaughter. PRV positive pre-smolts were found in about 36% of the freshwater cohorts and a general increase in viral load was observed after their transfer to seawater. A reduction in viral loads was recorded when fish approached slaughter (18 mo in sea cages). Sequencing of positive samples did not support the hypothesis that outbreaks are caused by the spreading of a particular (virulent) strain of PRV.

First detection of piscine reovirus (PRV) in marine fish species.

Heart and skeletal muscle inflammation (HSMI) is a disease that affects farmed Atlantic salmon Salmo salar L. several months after the fish have been transferred to seawater. Recently, a new virus called piscine reovirus (PRV) was identified in Atlantic salmon from an outbreak of HSMI and in experimentally challenged fish. PRV is associated with the development of HSMI, and has until now only been detected in Atlantic salmon. This study investigates whether the virus is also present in wild fish populations that may serve as vectors for the virus. The virus was found in few of the analyzed samples so there is probably a more complex relationship that involves several carriers and virus -reservoirs.