Alexander G. Murray

Epidemiological investigation into the re-emergence and control of an outbreak of infectious salmon anaemia in the Shetland Islands, Scotland.

Infectious salmon anaemia (ISA) is an orthomyxoviral disease, primarily affecting marine-phase farmed Atlantic salmon, which can result in high levels of mortality. ISA first emerged in Norway in the 1980s and subsequently has occurred in Canada, the USA, the Faeroe Islands and Chile. An outbreak occurred in Scotland in 1998-1999, but was eradicated at a cost of over pounds sterling 20M. The epidemiology of a new outbreak of ISA in the Scottish Shetland Islands during 2008-2009 is described. Six sites have been confirmed ISA-positive. Spread of the virus via transport of fish between marine sites, harvest vessels, smolts and wild fish appears to have been of little or no importance, with spread primarily associated with marine water currents. The use of management areas by Marine Scotland to control the event appears to have been effective in restricting spread to a small area. This localised outbreak contrasts with the 1998-1999 outbreak that spread over a wide geographic area with transported fish and harvest vessels. The development and application of industry codes of good practice, good husbandry and biosecurity practices, limited marine site-to-site movement of live fish and improved disinfection of vessels and processing plant waste that occurred subsequent to the 1998-1999 outbreak may explain the localised spread of infection in 2008-2009. Depopulation of confirmed sites has been achieved within 7 wk (mean = 3.7 wk); however, it is likely that subclinical infection persisted undetected for months on at least 1 site. The origin of the 2008-2009 outbreak remains unknown. Potential sources include evolution from a local reservoir of infection or importation. Synchronous fallowing of management areas, with good husbandry and biosecurity, reduces the risk of ISA recurring. Movement of fish between sites in different management areas represents the greatest risk of regional-scale spread, should this occur.

Using simple models to review the application and implications of different approaches used to simulate transmission of pathogens among aquatic animals

Disease is an important issue affecting aquatic animal populations. Aquatic pathogens may be transmitted in ways that could result in qualitatively different impacts to those of terrestrial diseases. I analyse simple SIR epidemic models with different functions to describe transmission. Four forms of transmission are applied: density-dependent, density-independent, non-linear density-dependent and constant infection pressure; the first two are similar to terrestrial systems, the second two are based on specifically aquatic modes of transmission. Observed diseases and existing models are reviewed in terms of these simple forms. The significance of mode of transmission to host populations, to strategies to prevent or control diseases, and to wild-farm interactions are analysed. Different diseases are simulated by different transmission models, for example furunculosis depends on host density, while spread of phocine distemper virus is density-independent, and sea lice infestation pressure may result from open transmission processes that are not dependent on local infested hosts. Appropriate transmission model may also depend on the scale of interest (inter- or intra-population). These different models result in very different responses to intervention strategies, for example culling may be effective for controlling density-dependent disease but may be counter-productive when pathogens depend on open recruitment. It is therefore important for management that appropriate models (whether existing or novel) be selected and this paper aims to provide a basic framework for cataloguing and management of aquatic diseases.

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 (β), 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 (β=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 β=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 β=0.10. These results demonstrate the potential benefits of having epidemiologically isolated management areas and applying synchronised fallowing.

Epidemiology of the spread of viral diseases under aquaculture.

Aquaculture production is increasing rapidly worldwide. However, production has been associated with the emergence of several novel diseases, including viral diseases, that have caused serious problems for producers. Using examples largely from salmon farming in Scotland I review briefly the factors that allow transmission to occur in aquaculture. These include transmission through the water, which is relatively local to the infected farm, and anthropogenic transports (such as transport of fish between sites) that may occur over very long distances. A Disease Management Area (DMA) approach, as developed in Scotland to fight infectious salmon anaemia, can be effective at reducing pathogen transmission and hence disease emergence.

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.

Modelling management strategies for a disease including undetected sub-clinical infection: Bacterial kidney disease in Scottish salmon and trout farms

Abstract Disease is a major constraint on animal production and welfare in agriculture and aquaculture. Movement of animals between farms is one of the most significant routes of disease transmission and is particularly hard to control for pathogens with subclinical infection. Renibacterium salmoninarum causes bacterial kidney disease (BKD) in salmonid fish, but infection is often sub-clinical and may go undetected with major potential implications for disease control programmes. A Susceptible-Infected model of R. salmoninarum in Scottish aquaculture has been developed that subdivides the infected phase between known and undetected sub-clinically infected farms and diseased farms whose status is assumed to be known. Farms officially known to be infected are subject to movement controls restricting spread of infection. Model results are sensitive to prevalence of undetected infection, which is unknown. However, the modelling suggests that controls that reduce BKD prevalence include improve biosecurity on farms, including those not known to be infected, and improved detection of infection. Culling appears of little value for BKD control. BKD prevalence for rainbow trout farms is less sensitive to controls than it is for Atlantic salmon farms and so different management strategies may be required for the sectors.

A game theory based framework for assessing incentives for local area collaboration with an application to Scottish salmon farming

Movements of water that transport pathogens mean that in net-pen aquaculture diseases are often most effectively managed collaboratively among neighbours. Such area management is widely and explicitly applied for pathogen management in marine salmon farms. Effective area management requires the active support of farm managers and a simple game-theory based framework was developed to identify the conditions required under which collaboration is perceived to be in their own best interest. The model applied is based on area management as practiced for Scottish salmon farms, but its simplicity allows it to be generalised to other area-managed net-pen aquaculture systems. In this model managers choose between purchasing tested pathogen-free fish or cheaper, untested fish that might carry pathogens. Perceived pay-off depends on degree of confidence that neighbours will not buy untested fish, risking input of pathogens that spread between farms. For a given level of risk, confidence in neighbours is most important in control of moderate-impact moderate-probability diseases. Common low-impact diseases require high confidence since there is a high probability a neighbour will import, while testing for rare high-impact diseases may be cost-effective regardless of neighbours actions. In some cases testing may be beneficial at an area level, even if all individual farms are better off not testing. Higher confidence is required for areas with many farms and so focusing management on smaller, epidemiologically imperfect, areas may be more effective. The confidence required for collaboration can be enhanced by the development of formal agreements and the involvement of outside disinterested parties such as trade bodies or government.

A comparison of modelling approaches to assess the transmission of pathogens between Scottish fish farms: the role of hydrodynamics and site biomass.

Scotland is the largest Atlantic salmon (Salmo salar) producer in the EU with an output of over 150,000 t, contributing over £500 million annually towards the economy. Production continues to increase, predominantly due to the increase in output per farm and reduction in losses due to infectious diseases. Farms are grouped within disease management areas whose boundaries are defined by where the closest pair of farms is separated by more than twice the tidal excursion distance (TE) Tidal excursion is defined as 7.2 km in mainland Scotland, or 3.6 km in the Shetland Islands). The majority of salmon farms are located within relatively sheltered inshore areas where non-tidal advective current speed is minimal. However there is an aspiration for offshore production where it might be possible to increase stocking levels and where current speeds will be greater so TE models could break down. Separation distances whereby farms would avoid infection risk were obtained using an analytical, discrete-time Susceptible-Exposed-Infectious-Recovered (SEIR) model coupled with a hydrodynamic transport expression representing transmission of pathogenic agents between fish farms. The model incorporated transmission, expression and recovery parameters as well as pathogen shedding and decay. The simplified hydrodynamic model incorporated residual advection, tidal advection and turbulent diffusion elements. The obtained separation distances were compared to a computationally intensive, numerical model and were demonstrated to be comparable, although the analytical model underestimated the variation within the transmission distances. Applying characteristics for a robust pathogen, infectious pancreatic necrosis virus type (IPNV-type), and less robust pathogens such as infectious salmon anaemia virus type (ISAV-type) and Aeromonas salmonicida type (AS-type) pathogens, it was possible to obtain separation distances whereby farms avoided infection. Simulation outputs indicated that separation distances should increase to avoid disease as farm size and current speed increase. The more conserved IPNV-type pathogen required separation distances of hundreds of kilometres, AS-type required tens of kilometres, whilst the distances for ISAV-type were within the scale of the current DMAs, that were developed for ISAV control. However, should production be moved to areas of faster moving currents and increased farm production the current disease management area principles might need readdressing.

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.

Increased frequency and changed methods in the treatment of sea lice (Lepeophtheirus salmonis) in Scottish salmon farms 2005–2011

BACKGROUND The sea louse is the most economically and environmentally serious ectoparasite of marine salmonids. Sea lice have been largely controlled by treatment with a variety of medicines. In order to understand the sustainability of medicine usage, an analysis of sea louse treatment data has been carried out for all Scottish salmon farms from 2005 to 2011. RESULTS Overall, there was an increase from 0.156 to 0.282 treatments month(-1) ; treatments could involve one or multiple agents. This increase was mostly in bath treatments (cypermethrin in 2007, largely replaced by deltamethrin and azamethiphos in 2008). Treatments using in-feed treatments (emamectin benzoate and teflubenzuron) increased only slowly. Treatments involving more than one medicine in a single month also increased, as did the probability of follow-up treatments. Treatments were seasonal, with peaks of in-feed treatments in March and August and bath treatments more frequent between August and December. CONCLUSION Frequency of sea louse treatment increased substantially, with an increase in multiagent and follow-up treatments. This increase in treatment activity is expensive to the industry and increases exposure of the neighbouring environment. This indicates that earlier louse control practices were not sustainable and so adapted.