Impacts of lice from fish farms on wild Scottish sea trout and salmon: summary of science

Summary of science relating to managing the risk of sea lice from fish farms affecting wild salmon and sea trout in Scotland.

The sea louse (Lepeophtheirus salmonis) is a native parasite that infects both farmed and wild salmonids to the detriment of aquaculture and is of concern to wild fisheries management and conservation interests (Torrissen et al. 2013). Recent reviews have considered interactions between sea lice from salmon farms and wild salmonids in detail (e.g. Taranger et al. 2015; Thorstad et al. 2015, Vollset et al. 2016). Here, a summary of the evidence from the peer-reviewed literature is presented, to inform assessment of the risk and effect of lice arising from salmon farms on Scottish wild salmonids. The aim is not to repeat existing reviews but to provide a succinct account of key information relevant to locating fish farms in the Scottish coastal zone. The science presented includes observational, experimental and modelling studies.

1. Salmon farms as sources of sea lice in the environment

In Scotland, salmon farms have been shown to be a much more important contributor than wild fish to the total numbers of sea lice in the Scottish coastal zone (Penston & Davies 2009).  Concentrations of larval lice sampled in areas near farms relate to the local farm lice loads (Penston & Davies 2009; Harte et al. 2017)  The numbers of lice found on salmon maintained in sentinel cages also relate to lice numbers reported on the nearest  farms (Pert et al. 2014, Salama et al. 2018).

2. Impacts of sea lice on sea trout

Under laboratory conditions, over 13 attached sea lice (at the pre-adult and adult mobile stages) per trout (19-70 g) caused physiological stress and was potentially lethal (Wells et al. 2006). However, in the wild, sea trout in coastal environments have the potential to return to fresh water, a behaviour that may act to remove lice but with physiological costs, including reduced growth (Halttunen et al. 2018; Serra-Llinares et al. 2020). Data collected throughout the west coast of Scotland showed that the proportion of individual sea trout with stress-inducing sea louse burdens increased with the mean weight of salmon on the nearest fish farm and decreased with distance from that farm (Middlemas et al. 2013; Shepherd et al. 2016). Levels of lice on wild sea trout also relate to fluctuations on farms associated with stage of production cycle (Middlemas et al. 2010). No information has yet been published to provide a quantitative estimate of the impact of lice on sea trout populations in Scotland.

3. Impacts of sea lice on wild salmon

3.1 Individual fish

Under laboratory conditions, mortality of individual salmon due to sea lice can occur at 0.2 mobile lice per g of host fish and becomes more likely as the level of infection increases (Fjelldal et al. 2020). Wild salmon smolts typically weigh in the range 10-80 g. Sub-lethal effects on salmon smolts due to sea lice include diminished liver energy reserves, impaired cardiac muscle, elevated stress responses and problems with osmoregulation (Medcalf et al. 2021; Fjelldal et al. 2020). Experiments in Norway, found that smolts treated against sea lice were larger when they returned as adults (Skilbrei et al. 2013).

3.2 Observational studies

Butler & Watt (2003) found densities of juvenile salmon to be lowest in west coast rivers near salmon aquaculture sites. Analysis of historical rod catch records from Scotland systematically allocated Scottish rivers into 3 areas: draining into the North sea, Irish sea, or Atlantic Ocean, which for west coast mainland rivers is via the Minches. Catches of wild salmon after the late 1980s declined on the Scottish Atlantic coast relative to elsewhere (Vøllestad et al. 2009). This area covers the majority of mainland Scotland’s salmon farms although the authors stressed that this did not prove a causative link with aquaculture. Ford & Myers (2008) compared indices of salmon abundance on the east and west coasts of Scotland together with farm production data. They found a relative reduction in the catches and counts of salmon on the west coast correlating with increased production of farmed salmon.

3.3 Experimental studies

Multiple studies conducted in Ireland and Norway using artificially reared salmon smolts have found that treatment with anti-sea lice agent increases likelihood of fish survival to return as adults (Vollset et al. 2016). The assumption from this is that protection of the emerging smolts from sea lice acquired in the coastal zone enhanced the ‘at sea’ survival. There is a great deal of year-to-year and site-to-site variation in the magnitude of such an effect; the reduction in numbers of returning salmon associated with lice in untreated smolts is in the range of 0-39%(Jackson et al. 2011; Krkošek et al. 2013; Skilbrei et al. 2013; Vollset et al. 2016). A Norwegian study where released salmon were exposed to various infection pressures (as determined by salmon held in sentinel cages) indicated that the difference between treated and control groups was associated with lice densities encountered in the environment (Bøhn et al. 2020).

Treatment and recapture studies in Scotland using wild smolts were not successful on the west coast due to the numbers of fish required. However, where sufficiently large numbers of smolts could be captured, such work could be performed when using infrastructure associated with large dams where identifying nearly all returning fish was possible (Morris et al. 2019a, b).

3.4 Modelling studies

Infection of wild salmonid smolts by sea lice emanating from salmon farms depends on environmental dispersal patterns and behaviours of sea lice and fish. The processes involved and associated best available biological data are combined in the model presented by Murray & Moriarty (2021) (Fig. 1).

Sea lice distribution in the environment can be  assessed by coupled hydrodynamic-particle models using appropriate biological and environmental data (Salama et al. 2018). Suitable hydrodynamic data is increasingly becoming available, such as from the Scottish Shelf Model (http://marine.gov.scot/themes/scottish-shelf-model).  Relevant biological data in the form of sea lice biology has been recently reviewed by Brooker et al. (2018) and sea lice biological models have also been described e.g. Salama et al. (2018). Testing of predictive lice dispersion models can be undertaken by observing infection pressure on smolts held in sentinel cages in relation to predicted larval lice distributions (Salama et al. 2018, Sandvik et al. 2020).

Fig. 1. Interaction of sea lice from farms with impact on wild salmonids (Murray and Moriarty 2021). Represented in the diagram are the processes that are combined to generate the potential impact on wild salmonid fish from lice arising from salmon farms. These processes are: (A) production of larval lice from adult female lice on farms; (B) distribution of these lice by currents; (C) exposure of wild salmonids; (D) impact of lice on these wild salmonids.

Modelling will always include uncertainties, as do field and experimental measurements. However, as techniques are updated and new data are collected, refinement of the models will provide increasingly accurate predictions of how sea lice are distributed as they emanate from an aquaculture site.

4. Distribution and movements of wild salmonid smolts

Susceptibility of salmonid smolts to lice from farms depends on where they are in space over time and how fast they move through areas where infective stages are present. Acoustic tracking of salmon smolts through upper Loch Linnhe has shown that the fish depart from their natal river and migrate toward sea at a median migration speed of 0.5 km per h [range 0.05-1.81] (Middlemas et al. 2018). Modelling (Ounsley et al. 2020) has demonstrated that directed swimming behaviour is required for smolts emigrating from the Scottish west coast to arrive at the shelf current which transports them to oceanic feeding grounds. Furthermore, swimming direction can greatly influence broad-scale distributions in relation to areas of aquaculture production. Currently no observational data are available regarding distribution and swimming speeds of salmon smolts having left loch systems on the west coast of Scotland.   

In acoustic tracking studies on the west coast, many sea trout remain near shore within sea lochs for at least their first two months at sea whereas some of them disperse more widely (Middlemas et al. 2009, 2018).

5. Mitigating Impacts

The risk of sea lice emanating from farms negatively affecting wild salmon and sea trout can be mitigated by 1) controlling release of lice larvae from the farms and 2) the strategic planning of farm locations.

The total number of lice on farms is a product of numbers of lice per fish and the number of farmed salmon. Generally numbers of lice per fish have declined since a recent peak in 2014-2016 (Hall and Murray 2018) due to application of a range of medicinal, biological and mechanical techniques on salmon farms (Toma et al. 2020). However, Scottish farmed salmon production has increased over the same period (Munro 2020).

Locating farms so that the accumulations of infective lice stages they produce avoid areas through which many salmon smolts migrate will reduce the risk of harm to the fish. Highest risk areas can be expected to include sea lochs with low natural flushing rates where smolts are constrained.

The location of farms relative to one another is also important due to potential for sea lice transfer between them, thereby increasing infection pressure. Models indicate that sea lice transport can occur over many tens of kilometres thereby linking production areas (Rabe et al. 2020). However, modelling in the Loch Linnhe system identified that >97% of sea lice are transported within 15 km of fish farms (Salama et al. 2016) and therefore local area management is likely to be beneficial for managing impact on wild salmon.

6. Conclusions

The body of scientific information indicates that there is a risk that sea lice from aquaculture facilities negatively affect populations of salmon and sea trout on the west coast of Scotland. Risks can be mitigated by reducing sea lice on farms or locating farms in areas that reduce interactions with wild salmonids. Potential for infection can be identified in broad terms using modelling approaches to assess likelihood of lice from farms infecting migrating salmon smolts. A growing information base is available to model distributions of sea lice emanating from salmon farms.

In view of uncertainties in available information, it is not a straightforward task to ascribe impact from a single farm to a specific wild salmonid population. When mitigating the risk posed to wild salmon and sea trout from sea lice emanating from salmon farms, an approach is needed that relates control of lice numbers on farms within a specified area to measured lice levels in the environment and estimation of associated risk. Such adaptive management is a useful approach where sustainable development of aquaculture is required.

References cited:

Bøhn T, Gjelland KØ, Serra-Llinares RM, Finstad B, Primicerio R, Nilsen R, Karlsen Ø, Sandvik AD, Skilbrei OT, Elvik KMS, Skaala O, Bjorn PA (2020) Timing is everything: Survival of Atlantic salmon Salmo salar post smolts during events of high salmon lice densities. Journal of Applied Ecology 57, 1149-1160.

Brooker AJ, Skern-Mauritzen R, Bron JE (2018) Production, mortality, and infectivity of planktonic larval sea lice, Lepeophtheirus salmonis (Krøyer, 1837): current knowledge and implications for epidemiological modelling. ICES Journal of Marine Research 75, 1214-1234.

Butler JRA, Watt J (2003) Wild salmonids and sea louse infestations on the west coast of Scotland: sources of infection and implications for the management of marine salmon farms. Pest Management Science 58, 595-608.

Fjelldal PG, Hansen TJ, Karlsen Ø (2020) Effects of laboratory salmon louse infection on osmoregulation, growth and survival in Atlantic salmon. Conservation Physiology 8, 1-10.

Ford JS & Myers RA (2008) A global assessment of salmon aquaculture impacts on wild salmonids. PLoS Biology, 6(2), e33

Gharbi K, Mathews, L, Bron, J, Roberts, R, Tinch, A, Stear M (2015) The control of sea lice in Atlantic salmon by selective breeding. Journal of the Royal Society Interface 12, 20150574

Hall LM, Murray AG (2018) Describing temporal change in adult female Lepeophtheirus salmonis abundance on Scottish farmed Atlantic salmon at the national and regional levels. Aquaculture 489, 148-153

Halttunen E, Gjelland KO, Hamel S, Serra-Llinares RM, Nilsen R, Arechavala-Lopez P, Skarohamar J, Johnsen IA, Asplin L, Karlsen O, Bjorn PA, Finstad B (2018) Sea trout adapt their migratory behaviour in response to high salmon lice concentrations. Journal of Fish Diseases 41, 953-967.

Harte AJ, Bowman AS, Salama NK, Pert CC (2017) Factors influencing the long-term dynamics of larval sea lice density at east and west coast locations in Scotland. Diseases of Aquatic Organisms 123, 181-192.

Jackson D, Cotter D, ÓMaoiléidigh N, O’Donohoe P, White J, Kane F, Kelly S, McDermott T, McEvoy S, Drumm A, Cullen A, Rogan G (2011) An evaluation of the impact of early infestation with the salmon louse Lepeophtheirus salmonis on the subsequent survival of outwardly migrating Atlantic salmon, Salmo salar L., smolts. Aquaculture 320, 159-163.

Krkošek M, Revie CW, Gargan PG, Skilbrei OT, Finstad B, Todd CD (2013) Impact of parasites on salmon recruitment in the Northeast Atlantic Ocean. Proceedings of the Royal Society Series B 280, 20122359.

Malcolm IA, Godfrey JD, Youngson AF (2010). Review of migratory routes and behaviour of Atlantic salmon, sea trout and European eel in Scotland's coastal environment: implications for the development of marine renewables. Scottish Marine and Freshwater Science 1, 14: 1-72. Available at http://www.scotland.gov.uk/Resource/Doc/295194/0111162.pdf.

Medcalf KE, Hutchings JA, Fast MD, Kuparinen A, Godwin SC (2021) Warming temperatures and ectoparasitic sea lice impair internal organs in juveniles Atlantic salmon. Marine Ecology Progress Series 660, 161-169.

Middlemas SJ, Stewart DC, Mackay S, Armstrong JD (2009) Habitat use and dispersal of post-smolt sea trout Salmo trutta in a Scottish sea loch system. Journal of Fish Biology 74, 639-651.

Middlemas SJ, Raffell JA, Hay DW, Hatton-Ellis M, Armstrong JD (2010) Temporal and spatial patterns of sea lice levels on sea trout in Western Scotland in relation to fish farm production cycles. Biology Letters 6, 548-551.

Middlemas SJ, Fryer RJ, Tulett D, Armstrong JD (2013) Relationship between sea lice levels on sea trout and fish farm activity in western Scotland. Fisheries Management and Ecology 20, 68–74.

Middlemas SJ, Stewart DJ, Henry JI, Wyndham M, Ballantyne L, Baum D (2018) Dispersal of post smolt Atlantic salmon and sea trout within a Scottish sea loch system. In Sea Trout, Science and Management: the proceedings of the 2nd international sea trout symposium. Ed Harris G. 339-353.

Morris DJ, Raynard RS, Armstrong JD, Collins C (2019a) SARFSP010 Piloting a network for determining spatial and temporal variation in marine survival of Atlantic salmon and effects of anti-sea lice agents. A study commissioned by the Scottish Aquaculture research forum (SARF).

Morris DJ, Gauld NR, Raynard R, Armstrong JD (2019b) A Pilot Study To Determine The Effect Of An Anti-Sea Lice Agent On The Marine Survival Of Atlantic Salmon On The West Coast Of Scotland. Scottish Marine and Freshwater Science Vol 10 No 5, 15pp. DOI: 10.7489/12212-1

Munro L (2020) Scottish fish farm production survey 2019. https://www.gov.scot/publications/scottish-fish-farm-production-survey-2019/

Murray AG, Moriarty M (2021) A simple modelling tool for assessing interaction with host and local infestation of sea lice from salmonid farms on wild salmonids based on processes operating at multiple scales in space and time. Ecological Modelling 443, 109459

Ounsely J.P., Gallego A., Morris D.J., Armstrong J.D. (2020) Regional variation in directed swimming by Atlantic salmon smolts leaving Scottish waters for their oceanic feeding grounds- a modelling study. ICES Journal of Marine Science 77,315-325.

Penston, M.J. & Davies, I.M. (2009) An assessment of salmon farms and wild salmonids as sources of Lepeophtheirus salmonis (Krøyer) copepodids in the water column in Loch Torridon, Scotland. Journal of Fish Diseases 32, 75-88.

Pert CC, Fryer RJ, Cook P, Kilburn R, McBeath S, McBeath A, Matejusova I, Urquhart K, Weir SJ, McCarthy U, Collins C, Amundrud T, Bricknell IR (2014). Using sentinel cages to estimate infestation pressure on salmonids from sea lice in Loch Shieldaig, Scotland. Aquaculture Environment Interactions 5, 49-59.

Rabe B, Gallego A, Wolf J, O’Hara Murray R, Struiver C, Price D, Johnson H (2020) Applied connectivity modelling at local to regional scale: The potential for sea lice transmission between Scottish finfish aquaculture management areas. Estuarine, Coastal and Shelf Science 238, 106716

Salama NKG, Dale AC, Ivanov VV, Cook PF, Pert CC, Collins CM, Rabe B (2018) Using biological-physical modelling for informing sea lice dispersal in Loch Linnhe, Scotland. Journal of Fish Diseases, 41, 901-919.

Salama NKG, Murray AG, Rabe B (2016) Simulated environmental transport distances of Lepeophtheirus salmonis in Loch Linnhe, Scotland for informing aquaculture area management structures. Journal of Fish Diseases, 39, 419-428.

Sandvik AD, Johnsen IA, Myksvoll MS, Sævik PN, Sogen MD 2020 Prediction of the salmon lice infestation pressure in a Norwegian fjord. ICES Journal of Marine Science, 77, 746-756.

Serra-Llinares RM, Bohn T, Karlsen O, Nilsen R, Freitas C, Albertsen J, Haraldstad T, Thorstad EB, Elvik KMS, Bjorn PA (2020) Impacts of salmon lice on mortality, marine migration distance and premature return in sea trout. Marine Ecology Progress Series 635, 151-168.

Skardhamar J, Fagerli MN, Reigstad M, Sandvik AD, Bjorn PA (2019) Sampling planktonic sea lice in Norwegian fjords. Aquaculture Environment Interactions 11, 701-715.

Shepherd S, MacIntyre C, Gargan P (2016) Aquaculture and environmental drivers of salmon lice infestation and body condition in sea trout. Aquaculture Environment Interactions 8, 597-610.

Skilbrei OT, Finstad B, Urdal K, Bakke G, Kroglund F, Strand R (2013) Impact of early salmon louse, Lepeophtheirus salmonis, infestation & differences in survival & marine growth of sea-ranched Atlantic salmon, Salmo salar L., smolts 1997-2009. Journal of Fish Diseases 36, 249–260.

Susdorf R, Salama NKG, Lusseau D (2018) Influence of body condition on the population dynamics of Atlantic salmon with consideration of the potential impact of sea lice. Journal of Fish Diseases 41, 941-951.

Taranger GL, Karlsen O, Bannister RJ, Glover KA, Husa V, Karlsbakk E, Kvamme BO, Boxaspen KK, Bjorn PA, Finstad B, Madhun AS (2015) Risk assessment of the environmental impact of Norwegian Atlantic salmon farming. ICES Journal of Marine Science 72, 997- 1021.

Thorstad EB, Todd CD, Uglem I, Bjorn PA, Gargan PG, Vollset KW, Halttunen E, Kalas S, Berg M, Finstad B (2015) Effects of salmon lice Lepeophtheirus salmonis on wild sea trout Salmo trutta- a literature review. Aquaculture Environment Interactions 7, 91-113.

Toma L, Shrestha S, Leinonen I, Boerlage A, Dverdal Jansen M, Crawford Revie C, Reeves, A 2020 Understanding the Relative Cost-Effectiveness of Sea Lice Management Measures for Farmed Salmon Production in Scotland.  Scottish Government, Edinburgh

Torrissen O, Jones S, Asche F, Gutormsen A, Skilbrei O, Nilsen F, Horsberg TE, Jackson D (2013) Salmon lice – impact on wild salmonids and salmon aquaculture. Journal of Fish Diseases 36, 171-194.

Vøllestad LA,Hirst D, L’Abée-Lund JH, Armstrong JD, MacLean JC, Youngson AF, Stenseth NC (2009) Divergent trends in anadromous salmonid populations in Norwegian and Scottish rivers. Proceedings of the Royal Society B series, 276, 1021-1027

Vollset KW, Barlaup, B T, Skoglund H, Normann ES, Skilbrei OT (2014) Salmon lice increase the age of returning Atlantic salmon. Biology Letters, 10:20130896.

Vollset, KW, Krontveit RI, Jansen PA, Finstad B, Barlaup BT, Skilbrei OT, Krkošek M, Romunstad P, Aunsmo A, Jensen AJ, Dohoo I (2016), Impacts of parasites on marine survival of Atlantic salmon: a meta-analysis. Fish and Fisheries. 17, 714-730.

Wells A, Grierson CE, MacKenzie M, Russon IJ, Reinardy H, Middlemiss C, Bjorn PA, Finstad B, Bonga SEW, Todd CD, Hazon N (2006) Physiological effects of simultaneous, abrupt seawater entry and sea lice (Lepeophtheirus salmonis) infestation of wild, sea- run sea trout (Salmo trutta) smolts. Canadian Journal of Fisheries and Aquatic Science. 63 2809-2821.