Association of ectoparasite Lepeophtheirus salmonis counts on farmed Atlantic salmon and wild sea trout in Scotland.

Parasitic sea lice (Copepoda: Caligidae) colonising marine salmonid (Salmoniformes: Salmonidae) aquaculture production facilities have been implicated as a possible pressure on wild salmon and sea trout populations. This investigation uses monitoring data from the mainland west coast and Western Isles of Scotland to estimate the association of the abundance of adult female Lepeophtheirus salmonis (Krøyer) colonising farmed Atlantic salmon Salmo salar L. with the occurrence of juvenile and mobile L. salmonis on wild sea trout, anadromous S. trutta L. The associations were evaluated using generalised linear mixed models incorporating farmed adult female salmon louse abundances which are temporally lagged relative to dependent wild trout values. The pattern of lags, which is consistent with time for L. salmonis development between egg and infective stage, was evaluated using model deviances. A significant positive association is identified between adult female L. salmonis abundance on farms and juvenile L. salmonis on wild trout. This association is consistent with a causal relationship in which increases in the number of L. salmonis copepodids originating from lice colonising farmed Atlantic salmon cause an increase of L. salmonis abundance on wild sea trout.

Modelling parasite impacts of aquaculture on wild fish: The case of the salmon louse (Lepeophtheirus salmonis) on out-migrating wild Atlantic salmon (Salmo salar) smolt.

For effective wild salmon (Salmo salar) conservation in areas where aquaculture of salmon is practiced it is necessary to identify where the key parasite, the salmon louse (Lepeophtheirus salmonis), will have an impact on these wild salmon. A simple modelling structure is implemented in a sample system in Scotland for assessing interaction between wild salmon and salmon lice from salmon farms. The model is demonstrated for case studies of smolt sizes and migration routes through salmon lice concentration fields derived for average farm loads from 2018 to 2020. Lice modelling describes production and distribution of lice, infection rates on hosts and biological development of lice. The modelling framework allows explicit assessment of the relationships between lice production, lice concentration and impact on hosts as they grow and migrate. Lice distribution in the environment is determined using a kernel model, which summarises mixing in a complex hydrodynamic system. Smolt modelling describes their initial size, growth and migration pathways. This is illustrated for a set of parameter values applied to 10 cm, 12.5 cm and 15 cm salmon smolts. We found that salmon lice impact depends on initial size of host, smaller smolts will be more susceptible, while larger smolts are less impacted by a given number of lice encounters and migrate more rapidly. This modelling framework can be adapted to allow evaluation of threshold concentrations of lice in the water that should not be exceeded to avoid impacts on smolt populations.

A preliminary assessment of indirect impacts on aquaculture species health and welfare in Scotland during COVID-19 lockdown.

COVID-19 led to sudden changes in human activities, mainly due to restrictive measures required to supress the virus. We assess the preliminary evidence for impacts on animal health and welfare in Scottish aquaculture, a key economic activity in remoter areas of the country. We summarise the industry structure, explore pathways of vulnerability to aquatic animal disease within a One Health framework that may be accentuated by impacts of COVID-19, and use basic routine data collection on the key welfare indicators of salmon mortality and parasitic sea lice counts. The indicators were published on schedule and provide no evidence of gross impact on health and welfare, at least for salmon, during the period of intensive lockdown restrictions in Scotland. Longer term effects cannot be ruled out and we do not assess impacts on the economic or social aspects of aquaculture production.

A GIS-based tool for an integrated assessment of spatial planning trade-offs with aquaculture.

The increasing demand for protein from aquaculture will trigger a global expansion of the sector in coastal and offshore waters. While contributing to food security, potential conflicts with other traditional activities such as fisheries or tourism are inevitable, thus calling for decision-support tools to assess aquaculture planning scenarios in a multi-use context. Here we introduce the AquaSpace tool, one of the first Geographic Information System (GIS)-based planning tools empowering an integrated assessment and mapping of 30 indicators reflecting economic, environmental, inter-sectorial and socio-cultural risks and opportunities for proposed aquaculture systems in a marine environment. A bottom-up process consulting more than 350 stakeholders from 10 countries across southern and northern Europe enabled the direct consideration of stakeholder needs when developing the GIS AddIn. The AquaSpace tool is an open source product and builds in the prospective use of open source datasets at a European scale, hence aiming to improve reproducibility and collaboration in aquaculture science and research. Tool outputs comprise detailed reports and graphics allowing key stakeholders such as planners or licensing authorities to evaluate and communicate alternative planning scenarios and to take more informed decisions. With the help of the German North Sea case study we demonstrate here the tool application at multiple spatial scales with different aquaculture systems and under a range of space-related development constraints. The computation of these aquaculture planning scenarios and the assessment of their trade-offs showed that it is entirely possible to identify aquaculture sites, that correspondent to multifarious potential challenges, for instance by a low conflict potential, a low risk of disease spread, a comparable high economic profit and a low impact on touristic attractions. We believe that a transparent visualisation of risks and opportunities of aquaculture planning scenarios helps an effective Marine Spatial Planning (MSP) process, supports the licensing process and simplifies investments.

Using the H-index to assess disease priorities for salmon aquaculture.

Atlantic salmon's (Salmo salar) annual aquaculture production exceeds 2M tonnes globally, and for the UK forms the largest single food export. However, aquaculture production is negatively affected by a range of different diseases and parasites. Effort to control pathogens should be focused on those which are most "important" to aquaculture. It is difficult to specify what makes a pathogen important; this is particularly true in the aquatic sector where data capture systems are less developed than for human or terrestrial animal diseases. Mortality levels might be one indicator, but these can cause a range of different problems such as persistent endemic losses, occasional large epidemics or control/treatment costs. Economic and multi-criteria decision methods can incorporate this range of impacts, however these have not been consistently applied to aquaculture and the quantity and quality of data required is large, so their potential for comparing aquatic pathogens is currently limited. A method that has been developed and applied to both human and terrestrial animal diseases is the analysis of published scientific literature using the H-index method. We applied this method to salmon pathogens using Web of Science searches for 23 pathogens. The top 3 H-indices were obtained for: sea lice, furunculosis, and infectious salmon anaemia; post 2000, Amoebic Gill Disease (AGD) replaced furunculosis. The number of publications per year describing bacterial disease declined significantly, while those for viruses and sea lice increased significantly. This reflects effective bacterial control by vaccination, while problems related to viruses and sea lice have increased. H-indices by country reflected different national concerns (e.g. AGD ranked top for Australia). Averaged national H-indices for salmon diseases tend to increase with log of salmon production; countries with H-Indices significantly below the trend line have suffered particularly large disease losses. The H-index method, supported by other literature analyses, is consistent with the nature and history of salmon diseases and so provides a useful quantitative measure for comparing different diseases in the absence of other measures.

Distribution of Infectious Pancreatic Necrosis Virus (IPNV) Based on Surveillance Programs in Freshwater Trout Farms of Mexico.

Diagnostic testing was performed between 2000 and 2012 to determine the distribution of infectious pancreatic necrosis virus (IPNV) in the main states of the Mexican Republic with freshwater Rainbow Trout Oncorhynchus mykiss (Walbaum) farms. This virus was positively identified from Rainbow Trout farms in seven of the eight states assessed. Due to nonnormal data distribution, a logistic regression model was applied for statistical analysis, the results of which indicated that virus prevalence was variable between states, with moderate but significant differences. Regarding the time periods evaluated, IPNV prevalence was higher during the first years of the study. The susceptible, infected, removed model was used to examine this phenomenon, which indicated that the decreased prevalence during the latter years of the study could be associated with a real elimination of the infection. The information of the cases analyzed also suggests a relationship with the irregularity in the submission of samples to the laboratory and emphasizes other factors that have contributed to the transmission of IPNV throughout the country. Received November 10, 2014; accepted December 5, 2015.

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.

Does the use of salmon frames as bait for lobster/crab creel fishing significantly increase the risk of disease in farmed salmon in Scotland?

Salmon farming is an important economic activity, and employer, particularly for remoter areas of Scotland; crustacean fisheries are also significant small businesses in these areas. Salmon frames (the head and spine that remain after evisceration and filleting) are sometimes used to bait the creel pots used to catch lobsters and crabs. These frames may contain pathogens that could potentially be spread to salmon farms in the vicinity of creel fisheries. Therefore, an analysis has been carried out for key pathogens of farmed salmon to assess the risks associated with this process. Infection of farms via creel bait requires that: (1) pathogens are present in salmon at harvest; (2) they are not removed from the salmon that used for bait during processing; (3) they transmit from creel pot baits to salmon farms. This last step is critical and leads to most of the uncertainty in results. Risk were assessed for 7 viruses, 3 bacteria, and 3 eukaryotic parasites of importance to salmon farming. A potentially significant risk was identified in association with disease control programmes if fish were filleted at a secondary processor; such a situation should arise only rarely. A very low risk, per event, was identified from imports, however, because of large numbers of Norwegian imports processed in the UK this risk is always present. Risks were at worst of low (disease control) or very low (imports) probability and are significant only because of the magnitude of consequences.

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.

Factors affecting variation in mortality of marine Atlantic salmon Salmo salar in Scotland.

Databases of site production have an important role to play in the investigation and understanding of diseases, since they store valuable amounts of disease and management data. Diseases pose an important constraint to economic expansion of aquaculture. They are dependent on the complex interacting factors of pathogen, environment, and host, and the causes of death can be related to nutritional, environmental, and genetic factors of the host or infectious agents. We examined the drivers of mortality from a single site-production database, which represented one-third of Scottish farmed salmon Salmo salar L. production in 2005, to determine whether mortality 'benchmarking' data could be generalised across sites and production cycles. We show that farm mortality records play an important role in studying mortality losses and identifying of management problems in production. We found that mortalities varied across the months of the year and with the time of year of initial stocking. Production cycles that started in the third quarter of the year had the highest mortality overall. Furthermore, we found site-to-site variation in mortality that may have been caused by either random occurrence of epidemics and environmental events or other local effects.

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.

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.

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

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.

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.

Persistence of infectious pancreatic necrosis virus (IPNV) in Scottish salmon (Salmo salar L.) farms.

Infectious pancreatic necrosis is a disease that is causing increasing loses to Scottish Atlantic-salmon farms. I asked the question: is infection of individual salmon farms persistent or transient? Using Fisheries Research Services' Fish Health Inspectors' data, conditional probabilities that a farm would (time 0) be infected were estimated for farms that had been infected [P(I(0)|I(-T))] or free [P(I(0)|F(-T))] from infectious pancreatic necrosis virus (IPNV) when a sample was taken at some earlier time (-T). A logistic-regression model was used to estimate these conditional probabilities with T; this model was multilevel to account for regional and inter-annual level differences in prevalence of IPNV. In freshwater, conditional probabilities remained substantially different for periods of at least 4 years, so, although many farms did change infection status, IPNV either persisted or recurred at specific freshwater farms. Marine farms showed similar conditional probabilities after about 2 years following a positive or a negative sample, indicating that infection was transient. Management of larger areas and exchanges between farms might be more effective than farm-level management at controlling marine IPNV.

A framework for understanding the potential for emerging diseases in aquaculture.

Numerous diseases have emerged as serious economic or ecological problems in aquaculture species. The combination of factors behind the emergence of each disease is unique, but various common factors are apparent. We combine risk-analysis methods and virulence theory with historical examples (mainly from salmonid production) to identify key disease-emergence risk factors. Diseases have emerged through pathogen exchange with wild populations, evolution from non-pathogenic micro-organisms and anthropogenic transfer of stocks. Aquacultural practices frequently result in high population densities and other stresses (such as intercurrent disease) which increase the risk of infection establishment and spread. As aquaculture expands and new species are farmed, diseases will continue to emerge and affect both wild and farmed fish adversely. The rate and extent of emergence can be reduced by the application of biosecurity programmes designed to mitigate the risk factors for disease emergence.

A model of spatially evolving herpesvirus epidemics causing mass mortality in Australian pilchard Sardinops sagax.

In 1995 mass mortality of pilchards Sardinops sagax occurred along >5000 km of Australian coast; similar events occurred in 1998/99. This mortality was closely associated with a herpesvirus. The pilchard is an important food source for larger animals and supports commercial fisheries. Both epidemics originated in South Australian waters and spread as waves with velocities of 10 to 40 km d(-1). Velocity was constant for a single wave, but varied between the epidemics and between the east- and west-bound waves in each epidemic. The pattern of mortality evolved from recurrent episodes to a single peak with distance from the origin. A 1-dimensional model of these epidemics has been developed. The host population is divided into susceptible, infected and latent, infected and infectious, and removed (recovered and dead) phases; the latent and infectious periods are of fixed duration. This model produces the mortality patterns observed locally and during the spread and evolution of the epidemic. It is consistent with evidence from pathology. The wave velocity is sensitive to diffusion coefficients, viral transmission rates and latent period. These parameters are constrained using the local and large-scale patterns of epidemic spread. The relative roles of these parameters in explaining differences between epidemics and between east- and west-bound waves within epidemics are discussed. The model predicts very high levels of infection, indicating that many surviving pilchards recovered following infection. Control appears impracticable once epidemics are initiated, but impact can be minimised by protecting juvenile stocks.

Infectious pancreatic necrosis virus in Scottish Atlantic salmon farms, 1996-2001.

The rapid growth of aquaculture has provided opportunities for the emergence of diseases. Programs designed to monitor these pathogens are useful for analysis of regional variation and trends, provided methods are standardized. Data from an official monitoring program were used to analyze the emergence of infectious pancreatic necrosis virus in Scottish salmon farms from 1996 to 2001. An annual increase in the prevalence of this virus was found in saltwater (10%) and freshwater sites (2% to 3%), with a much faster increase (6.5%) in Shetland's freshwater sites. No significant increase in the virus was detected in the marine farms of southern mainland Scotland. However, the virus had become very prevalent at marine sites and was almost ubiquitous in Shetland by 2001. The prevalence of this virus at marine sites may be underestimated. Because several diseases have emerged or are emerging in fish farming, aquaculture surveillance programs represent a rich potential source of data on emerging diseases.

Using observed load distributions with a simple model to analyse the epidemiology of sea lice (Lepeophtheirus salmonis) on sea trout (Salmo trutta).

Sea lice are ectoparasites of salmonids that have been associated with the recent decline in sea trout numbers in north-west Europe. Observed patterns of louse load distribution between sea trout in the seas surrounding the UK, Ireland and Norway and a simple model have been used to analyse the epidemiology of lice. Loads are aggregated and deviate strongly from the Poisson distribution, although less than is observed with many other parasites. The louse numbers on fish from offshore sites are slightly less variable than for fish from coastal sites with comparable mean loads. Analysis of louse development stages and sexes shows that selection between hosts by sea lice plays a limited role. If host selection is absent, then associated poor condition would be caused by, not the cause of, high louse burdens; however the absence of such selection is not proved. Scenarios with infection that is patchy in space and time best generate the aggregated load patterns observed; these patches accord with observed swarms of copepodids. Prevalence patterns may indicate the movement of trout between environments. Control of copepodids in infection 'hot spots', either directly or through control of louse egg production in their catchment, may reduce louse loads on wild sea trout and, in particular, extreme and damaging loads.