Infestation rates of lice Lepeophtheirus salmonis and Caligus elongatus on Atlantic salmon in fixed and towed sentinel cages.

Sea lice are a key limitation to sustainable salmon aquaculture, and effective monitoring strategies are critical for the management of these parasites. Sentinel cages are an established means of assessing infestation pressure at fixed locations, but as smolts move through systems they will be exposed to varying lice densities. As a means of assessing infestation pressure along trajectories, we describe the development and application of towed sentinel cages (TSCs) in a Scottish sea loch containing salmonid aquaculture. Trial deployments took place over 3 yr (2016-2018), and levels of sea lice infestation were compared between methodologies. Oceanographic data was collected alongside TSCs to put the results into the environmental context that smolts and sea lice experienced during the tows. The sea lice infestation rates found from TSCs were comparable to those on contemporaneously deployed fixed sentinel cages. Thus, due to their practicability and consistency with other surveillance methods, TSCs could be used to improve the assessment of exposure risk along wild salmonid smolt migration trajectories, where these are known.

Modelling temperature and fish biomass data to predict annual Scottish farmed salmon, Salmo salar L., losses: Development of an early warning tool.

Losses due to mortality are a serious economic drain on Scottish salmon aquaculture and are a limitation to its sustainable growth. Understanding the changes in losses, and associated drivers, are required to identify risks to sustainable aquaculture. Data on losses were obtained from two open source data sets: monthly losses of biomass 2003-2018 and losses of salmon over production cycles (numbers input minus output harvest) 2002-2016. Monthly loss rates increased, accelerating after 2010, while losses per production cycle displayed no trend. Two modelling frameworks were investigated to produce an early warning tool for managers about potential increases in losses. Both linear regression and beta regression showed that monthly losses related to biomass and minimum winter air temperatures with high precision and low bias. These relationships apply at both the national and regional levels where the beta regression best fit model explain 82 % and 69 % of variation in mortality, some regional differences apply, particularly for the Northern Isles. The lack of trend in losses per production cycle may have been due to shorter production cycles as more salmon were harvested earlier, and possibly increasing losses of larger salmon (which affects biomass but not numbers lost). In the long-term, the models predict that milder winters and increased biomass will be associated with increased mortality, which will need to be managed. In the short-term, given relatively little year-to-year variation in biomass, minimum winter temperature is a powerful early warning of the likely extent of losses in the Scottish salmon farming industry.

The contact structure of Great Britain's salmon and trout aquaculture industry.

We analyse the network structure of the British salmonid aquaculture industry from the perspective of infectious disease control. We combine for the first time live fish transport (or movement) data covering England and Wales with data covering Scotland and include network layers representing potential transmission by rivers, sea water and local transmission via human or animal vectors in the immediate vicinity of each farm or fishery site. We find that 7.2% of all live fish transports cross the England-Scotland border and network analysis shows that 87% of English and Welsh nodes and 72% of Scottish nodes are reachable from cross-border connections via live fish transports alone. Consequently, from a disease-control perspective, the contact structures of England and Wales and of Scotland should not be considered in isolation. We also show that large epidemics require the live fish movement network and so control strategies targeting movements can be very effective. While there is relatively low risk of widespread epidemics on the live fish transport network alone, the potential risk is substantially amplified by the combined interaction of multiple network layers.

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.

A Modelling Framework for Assessing the Risk of Emerging Diseases Associated with the Use of Cleaner Fish to Control Parasitic Sea Lice on Salmon Farms.

Sea lice are the most damaging parasite of marine salmonids, both economically and in terms of potential impacts on wild fish. An increasingly widely applied control is the use of cleaner fish (CF) such as wrasse that eat lice. However, such CF can carry pathogens that may cause disease in salmon, including the potential emergence of new diseases. This is not just a theoretical risk, as demonstrated by a recent outbreak of viral haemorrhagic septicaemia in wrasse held on salmon farms in Shetland. A modelling framework is developed to identify conditions in which emergence might occur, and, from this, means of reducing risk. Diseases that might emerge easily in farmed salmon would be likely to have already done so by other routes of exposure, and if risks are very low, they would need to be greatly enhanced to become significant relative to costs of lice control. CF may most enhance risks from disease with moderate probability of emerging. Risks of emergence can be reduced by replacing wild-caught with hatchery-reared CF, minimizing mixing of CF from different sources, surveillance for clinical disease in the CF and ensuring strategic biosecurity (area management with synchronized fallowing). Reuse of CF for a second salmon production cycle may reduce costs and even probability of infection (especially from wild-caught CF), but should only be considered as part of a rigorous area management programme because the practice presents opportunities for pathogens to adapt to salmon by weakening fallowing.

Simulated environmental transport distances of Lepeophtheirus salmonis in Loch Linnhe, Scotland, for informing aquaculture area management structures.

In the majority of salmon farming countries, production occurs in zones where practices are coordinated to manage disease agents such as Lepeophtheirus salmonis. To inform the structure of zones in specific systems, models have been developed accounting for parasite biology and system hydrodynamics. These models provide individual system farm relationships, and as such, it may be beneficial to produce more generalized principles for informing structures. Here, we use six different forcing scenarios to provide simulations from a previously described model of the Loch Linnhe system, Scotland, to assess the maximum dispersal distance of lice particles released from 12 sites transported over 19 day. Results indicate that the median distance travelled is 6.1 km from release site with <2.5% transported beyond 15 km, which occurs from particles originating from half of the release sites, with an absolute simulated distance of 36 km observed. This provides information suggesting that the disease management areas developed for infectious salmon anaemia control may also have properties appropriate for salmon lice management in Scottish coastal waters. Additionally, general numerical descriptors of the simulated relative lice abundance reduction with increased distance from release location are proposed.

An approach to evaluating the reliability of diagnostic tests on pooled groups of infected individuals.

An experimental design and statistical analysis providing information on the reliability of pooled test procedures is described. It involves estimating the relationship between the probability of a positive pooled test result (dependent variable) and the expected number of infected individuals in a pool (explanatory variable). The intercept is an estimate of the proportion of false positives (1-pooled specificity) and pooled sensitivities can be estimated for indicative prevalences of infected individuals. Simulations for a theoretical infection are used to investigate the advantages and limitations of the approach. The approach is used to evaluate the reliability of a virus isolation and qRT-PCR test procedure detecting Salmonid alphavirus the pathogenic agent necessary for the development of Pancreas Disease in Atlantic salmon (Salmo salar).

Development and assessment of a biophysical dispersal model for sea lice.

Salmon aquaculture in Scotland continues to increase; however, one of the potential limitations to its further sustainable growth is the ectoparasitic sea louse Lepeophtheirus salmonis. The industry in Scotland undertakes coordinated management procedures to control the levels of sea lice on farms in designated production areas. We developed a biophysical sea lice dispersal model for Loch Linnhe, one of the largest fjords on the west coast of Scotland, to provide further information to help establish more effective farm management areas. We successfully extend modelling principles previously applied to a small Scottish fjordic system. Modelling scenarios demonstrate heterogeneity in the distribution of sea lice within the system and simulations, suggesting that lice could be transmitted up to 30 km. The scenarios are assessed by comparing model predictions against lice sampled by both planktonic trawls and settlement on sentinel caged fish. The model predicts the ranked abundance of both planktonic and settled lice assuming that the lice input to the system is relative to host biomass. Data collection is ongoing for undertaking and assessing additional scenarios.

Seasonality and heterogeneity of live fish movements in Scottish fish farms.

Movement of live animals is a key contributor to disease spread. Farmed Atlantic salmon Salmo salar, rainbow trout Onchorynchus mykiss and brown/sea trout Salmo trutta are initially raised in freshwater (FW) farms; all the salmon and some of the trout are subsequently moved to seawater (SW) farms. Frequently, fish are moved between farms during their FW stage and sometimes during their SW stage. Seasonality and differences in contact patterns across production phases have been shown to influence the course of an epidemic in livestock; however, these parameters have not been included in previous network models studying disease transmission in salmonids. In Scotland, farmers are required to register fish movements onto and off their farms; these records were used in the present study to investigate seasonality and heterogeneity of movements for each production phase separately for farmed salmon, rainbow trout and brown/sea trout. Salmon FW-FW and FW-SW movements showed a higher degree of heterogeneity in number of contacts and different seasonal patterns compared with SW-SW movements. FW-FW movements peaked from May to July and FW-SW movements peaked from March to April and from October to November. Salmon SW-SW movements occurred more consistently over the year and showed fewer connections and number of repeated connections between farms. Therefore, the salmon SW-SW network might be treated as homogeneous regarding the number of connections between farms and without seasonality. However, seasonality and production phase should be included in simulation models concerning FW-FW and FW-SW movements specifically. The number of rainbow trout FW-FW and brown/sea trout FW-FW movements were different from random. However, movements from other production phases were too low to discern a seasonal pattern or differences in contact pattern.

The effectiveness of fallowing strategies in disease control in salmon aquaculture assessed with an SIS model.

Salmon production is an important industry in Scotland, with an estimated retail value >£1 billion. However, this salmon industry can be threatened by the invasion and spread of diseases. To reduce this risk, the industry is divided into management areas that are physically separated from each other. Pathogens can spread between farms by local processes such as water movement or by long-distance processes such as live fish movements. Here, network modelling was used to investigate the importance of transmission routes at these two scales. We used different disease transmission rates (ß), where infected farms had the probability of 0.10, 0.25 or 0.50 per month to infect each contacted farm. Interacting farms were modelled in such a way that neighbours within a management area could infect each other, resulting in two contacts per farm per month. In addition, non-local transmission occurred at random. Salmon are input to marine sites where they are raised to harvest size, the site is then fallowed; in the model the effects of different fallowing strategies (synchronised, partial synchronised and unsynchronised fallowing at the management area level) on the emergence of diseases were investigated. Synchronised fallowing was highly effective at eradicating epidemics when transmission rate is low (ß=0.10) even when long distance contacts were fairly common (up to 1.5farm(-1)month(-1)). However for higher transmission rates, long distance contacts have to be kept at much lower levels (0.15contactsmonth(-1) where ß=0.25) when synchronised fallowing was applied. If fallowing was partially synchronised or unsynchronised then low rates of long-distance contact are required (0.75 or 0.15farm(-1)month(-1)) even if ß=0.10. These results demonstrate the potential benefits of having epidemiologically isolated management areas and applying synchronised fallowing.

An experimental investigation on aspects of infectious salmon anaemia virus (ISAV) infection dynamics in seawater Atlantic salmon, Salmo salar L.

This study investigated infection dynamics of infectious salmon anaemia virus (ISAV) by conducting two experiments to examine minimum infective dose and viral shedding of ISAV. In terms of minimum infective dose, the high variability between replicate tanks and the relatively slow spread of infection through the population at 1 x 10(1) TCID(50) mL(-1) indicated this dose is approaching the minimum infective dose for ISAV in seawater salmon populations. A novel qPCR assay incorporating an influenza virus control standard with each seawater sample was developed that enabled the quantity of ISAV shed from infected populations to be estimated in values equivalent to viral titres. Viral shedding was first detected at 7 days post-challenge (5.8 x 10(-2) TCID(50) mL(-1)kg(-1)) and rose to levels above the minimum infective dose (4.2 x 10(1) TCID(50) mL(-1)kg(-1)) on day 11 post-challenge, 2 days before mortalities in ISAV inoculated fish started. These results clearly demonstrate that a large viral shedding event occurs before death. Viral titres peaked at 7.0 x 10(1) TCID(50) mL(-1)kg(-1) 15 days post-infection. These data provide important information relevant to the management of ISA.

Modelling sea lice dispersion under varying environmental forcing in a Scottish sea loch.

The spread of infectious larval sea lice, Lepeophtheirus salmonis (Krøyer, 1838), between wild salmonids and farmed Atlantic salmon, Salmo salar, remains a contentious area of uncertainty. However, as laboratory and field experiments increase our knowledge of sea lice behaviour under environmental forcing, numerical modelling tools can be used to predict the spread of infectious sea louse larvae from a point source. A three-dimensional numerical model has been developed and recently validated within Loch Torridon, a fjordic sea loch on the west coast of Scotland. Output from the numerical model is used to drive a particle tracking model which follows statistical representations of sea lice through the planktonic stages of a louse life cycle. By including maturation and mortality, the models can be used to predict the dispersion and transport of infectious sea lice from a point source and can be used to produce maps of infectivity under varying environmental conditions. Results highlight the importance of the wind-driven circulation for larval lice transport and suggest that local environmental conditions have considerable impact on the probability of sea lice infection spreading between wild and farmed fish populations.

Estimation of infectious dose and viral shedding rates for infectious pancreatic necrosis virus in Atlantic salmon, Salmo salar L., post-smolts.

Infectious dose and shedding rates are important parameters to estimate in order to understand the transmission of infectious pancreatic necrosis virus (IPNV). Bath challenge of Atlantic salmon post-smolts was selected as the route of experimental infection as this mimics a major natural route of exposure to IPNV infection. Doses ranging from 10(2) to 10(-4) 50% end-point tissue culture infectious dose (TCID(50)) mL(-1) sea water were used to estimate the minimum infectious dose for a Scottish isolate of IPNV. The minimum dose required to induce infection in Atlantic salmon post-smolts was <10(-1) TCID(50) mL(-1) by bath immersion (4 h at 10 degrees C). The peak shedding rate for IPNV following intraperitoneal challenge using post-smolts was estimated to be 6.8 x 10(3) TCID(50) h(-1) kg(-1) and occurred 11 days post-challenge. This information may be incorporated into mathematical models to increase the understanding of the dispersal of IPNV from marine salmon sites.

Existing and potential use of models in the control and prevention of disease emergencies affecting aquatic animals.

Models are tools that aid managers to make decisions in a transparent manner. Models are implicitly used to devise any management plan, but scientific modelling makes the approach explicit and transparent. Simple models are often more useful than complex models, especially when time and data are short--as in many emergency situations. Four areas in which modelling can help aquatic animal health managers to control or prevent disease emergencies are identified, and their application reviewed. These areas are: models of factors behind disease outbreaks; models for the design of efficient surveillance; models of disease spread (subdivided into Susceptible-Infected-Removed [SIR] models, coupled hydrodynamic-particle transport models and network models); and models to evaluate the consequences of disease outbreaks. Import risk analysis and SIR modelling have been applied fairly extensively; risk-based surveillance is likely to be a driver for increased modelling effort in the near future.

Distribution of infectious pancreatic necrosis virus (IPNV) in wild marine fish from Scottish waters with respect to clinically infected aquaculture sites producing Atlantic salmon, Salmo salar L.

This study represents the first large-scale investigation of IPNV in Scottish wild marine fish. Kidney samples were taken from 30 627 fish comprising 37 species and 45 isolations were made from nine different species, illustrating these as reservoirs of IPNV in Scottish waters. The estimated prevalence of IPNV in the Scottish marine environment was low at 0.15% (90% confidence intervals, (CI) of 0.11-0.19%). This was significantly greater in fish caught less than 5.0 km from IPN-positive fish farms in Shetland, at 0.58% (90% CI of 0.45-0.77%). This prevalence persisted and did not significantly decrease over the 16-month period of study. The estimated prevalence of IPNV for each positive species was less than 1% with the statistically non-significant exceptions of flounder, Platichthys flesus (L.), at 12.5% (90% CI of 0.64-47.06%) and saithe, Pollachius virens (L.), at 1.11% (90% CI of 0.49-2.19%). The 45 isolates were titrated and all but two were below the detection limit of the test (<55 PFU g(-1)). Titres of 3.8 x 10(2) PFU g(-1) and 2.8 x 10(1) PFU g(-1) were calculated from common dab, Limanda limanda (L.), and saithe, respectively. This study provides evidence that clinical outbreaks of IPN in farmed Atlantic salmon may cause a localized small increase in the prevalence of IPNV in wild marine fish.

The application of risk analysis in aquatic animal health management.

Risk analysis has only been regularly used in the management of aquatic animal health in recent years. The Agreement on the Application of Sanitary and Phytosanitary measures (SPS) stimulated the application of risk analysis to investigate disease risks associated with international trade (import risk analysis-IRA). A majority (9 of 17) of the risk analyses reviewed were IRA. The other major focus has been the parasite of Atlantic salmon--Gyrodactylus salaris. Six studies investigated the spread of this parasite, between countries, rivers and from farmed to wild stocks, and clearly demonstrated that risk analysis can support aquatic animal health policy development, from international trade and biosecurity to disease interaction between wild and farmed stocks. Other applications of risk analysis included the spread of vertically transmitted pathogens and disease emergence in aquaculture. The Covello-Merkhofer, risk analysis model was most commonly used and appears to be a flexible tool not only for IRA but also the investigation of disease spread in other contexts. The limitations of the identified risk assessments were discussed. A majority were qualitative, partly due to the lack of data for quantitative analysis, and this, it can be argued, constrained their usefulness for trade purposes (i.e. setting appropriate sanitary measures); in other instances, a qualitative result was found to be adequate for decision making. A lack of information about the disease hazards of the large number of fish species traded is likely to constrain quantitative analysis for a number of years. The consequence assessment element of a risk analysis was most likely to be omitted, or limited in scope and depth, rarely extending beyond examining the evidence of susceptibility of farmed and wild species to the identified hazard. The reasons for this are discussed and recommendations made to develop guidelines for a consistent, systematic and multi-disciplinary approach to consequence assessment. Risk analysis has improved decision making in aquatic animal health management by providing a transparent method for using the available scientific information. The lack of data is the main constraint to the application of risk analysis in aquatic animal health. The identification of critical parameters is an important output from risk analysis models which should be used to prioritise research.

Modelling for disease preparedness and response.

Modelling is a useful tool for the understanding and hence, potentially, control of disease. In an emergency situation, obtaining data to validate detailed models may be difficult. However, modelling can be useful in aiding the management of disease, if the objectives are not too ambitious. For example, import risk analysis can use models to minimise the risk of outbreaks. Modelling can also be used to maximise the power of surveillance data to ensure that any outbreak is detected as rapidly as possible. Methods of modelling spread of disease, and measures to prevent this, including SIR-style epidemiological models, models of disease control zones and contact network models can be used to identify and minimise the potential scale of an epidemic. Finally, economic and ecological models can be used to assess the impact of outbreaks. A range of simple models is likely to be of more use than a single comprehensive model.