Prevention not cure: a review of methods to avoid sea lice infestations in salmon aquaculture

Abstract

The Atlantic salmon aquaculture industry still struggles with ectoparasitic sea lice despite decades of research and development invested into louse removal methods. In contrast, methods to prevent infestations before they occur have received relatively little research effort, yet may offer key benefits over treatment-focused methods. Here, we summarise the range of potential and existing preventative methods, conduct a meta-analysis of studies trialling the efficacy of existing preventative methods, and discuss the rationale for a shift to the prevention-focused louse management paradigm. Barrier technologies that minimise host-parasite encounter rates provide the greatest protection against lice, with a weighted median 76% reduction in infestation density in cages with plankton mesh ‘snorkels’ or ‘skirts’, and up to a 100% reduction for fully enclosed cages. Other methods such as geographic spatiotemporal management, manipulation of swimming depth, functional feeds, repellents, and host cue masking can drive smaller reductions that may be additive when used in combination with barrier technologies. Finally, ongoing development of louse-resistant salmon lineages may lead to long term improvements if genetic gain is maintained, while the development of an effective vaccine remains a key target. Preventative methods emphasise host resistance traits while simultaneously reducing host-parasite encounters. Effective implementation has the potential to dramatically reduce the need for delousing and thus improve fish welfare, productivity and sustainability in louse-prone salmon farming regions.

Full text

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
1
Prevention not cure: a review of methods to avoid sea lice infestations in salmon
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aquaculture
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Luke T Barrett 1*, Frode Oppedal 2, Nick Robinson 1,3, Tim Dempster 1
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1 Sustainable Aquaculture Laboratory – Temperate and Tropical (SALTT), School of
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BioSciences, University of Melbourne, Australia
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2 Animal Welfare Group, Institute of Marine Research, Matre Research Station, Matredal,
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Norway
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3 Breeding and Genetics, Nofima, Ås, Norway
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*Corresponding author: luke.barrett@unimelb.edu.au
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ORCIDs:
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LB: 0000-0002-2820-0421
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NR: 0000-0003-1724-2551
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TD: 0000-0001-8041-426X
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Key words: sea louse; Lepeophtheirus salmonis; Caligus spp.; Salmo salar; control
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Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
2
ABSTRACT
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The Atlantic salmon aquaculture industry still struggles with ectoparasitic sea lice despite
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decades of research and development invested into louse removal methods. In contrast,
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methods to prevent infestations before they occur have received relatively little research
24
effort, yet may offer key benefits over treatment-focused methods. Here, we summarise the
25
range of potential and existing preventative methods, conduct a meta-analysis of studies
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trialling the efficacy of existing preventative methods, and discuss the rationale for a shift to
27
the prevention-focused louse management paradigm. Barrier technologies that minimise host-
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parasite encounter rates provide the greatest protection against lice, with a weighted median
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76% reduction in infestation density in cages with plankton mesh ‘snorkels’ or ‘skirts’, and
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up to a 100% reduction for fully enclosed cages. Other methods such as geographic
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spatiotemporal management, manipulation of swimming depth, functional feeds, repellents,
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and host cue masking can drive smaller reductions that may be additive when used in
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combination with barrier technologies. Finally, ongoing development of louse-resistant
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salmon lineages may lead to long term improvements if genetic gain is maintained, while the
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development of an effective vaccine remains a key target. Preventative methods emphasise
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host resistance traits while simultaneously reducing host-parasite encounters. Effective
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implementation has the potential to dramatically reduce the need for delousing and thus
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improve fish welfare, productivity and sustainability in louse-prone salmon farming regions.
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INTRODUCTION
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The global expansion of sea cage fish farming has driven considerable shifts in the population
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dynamics of marine pathogens. For 40 years, ectoparasitic lice have been an intractable
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problem for Atlantic salmon (Salmo salar) farming industries in Europe and the Americas
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(Torrissen et al. 2013; Iversen et al. 2015). Louse infestations are almost ubiquitous on
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salmon farms in these regions – primarily the salmon louse Lepeophtheirus salmonis but also
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Caligus elongatus in the northern hemisphere, and Caligus rogercresseyi in South America
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(Hemmingsen et al. 2020). Lice are natural parasites of fish, but intensive salmon farming
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amplifies louse densities, resulting in unnaturally high infestation pressure for both farmed
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and wild salmonids. Lice feed on the skin, blood and mucus of host fish, and severe
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infestations can cause ulceration leading to stress, osmotic imbalance, anaemia and bacterial
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infection (Grimnes and Jakobsen 1996; Øverli et al. 2014; González et al. 2016).
52

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sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
3
Accordingly, management of louse infestations on farmed fish is crucial to maintain
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acceptable stock welfare, limit production losses and reduce impacts on adjacent wild
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salmonid populations (Krkošek et al. 2013; Thorstad et al. 2015).
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In most jurisdictions, the primary management approach is to monitor louse densities on
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farmed fish, with mandatory delousing or other sanctions implemented when louse levels
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exceed allowable limits. Regulations also cap the number of active sites or total biomass in
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each management zone according to estimated infestation pressure on wild salmonids, and
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may mandate coordinated fallowing or other measures (e.g. Norway: Ministry of Trade and
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Fisheries, 2012). The introduction of chemotherapeutants in the 1970s allowed farms to treat
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sea louse infestations without substantially reducing production (Aaen et al. 2015). However,
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most chemotherapeutants are not environmentally benign, leading to concerns about
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bioaccumulation and effects on non-target invertebrate species (Burridge et al. 2010). More
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recently, treatment-resistant lice have emerged on farms in Europe and the Americas (Aaen et
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al. 2015) rendering many chemotherapeutants less effective.
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The discovery of treatment-resistance has prompted a rapid and recent shift to mechanical
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and thermal delousing methods in the Norwegian salmon farming industry (Overton et al.
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2018), with these methods also gaining traction elsewhere (e.g. Canada, Chile, Scotland).
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Mechanical and thermal delousing are highly effective at removing mobile lice and have little
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or no impact on non-target species. However, they are stressful for host fish and can lead to
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elevated post-treatment mortality rates compared to the use of chemotherapeutants (Overton
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et al. 2018). Low salinity or hydrogen peroxide baths are also effective in the right conditions
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and do not accumulate, although the long-term prospects for these methods are uncertain
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given the possibility of increasingly resistant lice (Treasurer et al. 2000, Helgesen et al. 2018,
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Groner et al. 2019). Alternatively, around 50 million cleaner fish (lumpfish Cyclopterus
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lumpus and several wrasse species) are deployed annually at Norwegian salmon farms to eat
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lice directly off salmon (Norwegian Directorate of Fisheries 2018), with >1.5 million cleaner
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fish also used in Scotland (Marine Scotland Directorate, 2017). However, it is unclear
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whether their efficacy (Overton et al. 2020; Barrett et al. 2020a) is sufficient to justify their
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poor welfare in commercial sea cages (Nilsen et al. 2014; Hvas et al. 2018; Mo and Poppe
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2018; Yuen et al. 2019; Stien et al. 2020).
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Decades of innovation in louse control have allowed the salmon farming industry to continue
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functioning in louse-prone regions, but not without significant environmental and ethical
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concerns. Most research and development efforts so far have focused on treating at the post-
85

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
4
infestation stage. This likely reflects the relatively rapid return on investment into new
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delousing methods but may be a sub-optimal strategy if opportunities to invest in long term
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solutions are missed (Brakstad et al. 2019). An alternative approach is to focus louse
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management efforts on preventing infestation via proactive interventions (‘preventative
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methods’ herein) that may significantly reduce the need for farms to delouse. Here, we
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summarise the range of potential or existing preventative methods and conduct a meta-
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analysis of empirical estimates of sea louse removal efficacy for each method. Finally, we
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discuss the rationale for a paradigm shift from reactive louse control to a proactive approach
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that focuses on predicting and preventing infestations, and outline some possible strategies to
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promote long term efficacy of preventative methods.
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WHAT PREVENTATIVE METHODS ARE AVAILABLE?
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Preventative methods are deployed pre-emptively to reduce the rate of new infestations.
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Within this classification, we include approaches that either: (1) reduce encounter rates
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between salmon and infective copepodid stage lice; or (2) reduce the attachment success
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and/or early post-settlement survival of copepodids via interventions that begin to act at the
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moment of attachment or first feeding (Fig. 1). These approaches are distinct from control via
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delousing treatments, which are generally implemented as a reaction to an existing infestation
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(i.e. ‘immediate’ control), or via cleaner fish, which may be deployed prior to infestation and
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function on an ongoing basis (i.e. ‘continuous’ control) but are not typically effective against
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newly attached lice (e.g. Imsland et al. 2015).
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1. Reducing encounters
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1.1 Barrier technologies
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A growing understanding of louse physiology and host-finding behaviour has led to several
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important advances in louse prevention, and by using data on preferred swimming depths of
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infective copepodids in relation to environmental parameters (Heuch 1995; Heuch et al.
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1995; Crosbie et al. 2019), farmers can now separate hosts from parasites using depth-
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specific louse barriers.
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Barriers made from fluid-permeable plankton mesh or impermeable membranes can
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dramatically reduce infestation rates by preventing infective copepodids from entering the
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cage environment. ‘Skirt’ or ‘snorkel’ barriers prevent particles in the surface layers—where
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most copepodids reside—from entering the cage while still allowing full water exchange
117

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
5
below the level of the barrier (Oppedal et al. 2017; Wright et al. 2017; Stien et al. 2018).
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Salmon often choose to reside below the level of the skirt or snorkel, meaning that the barrier
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functions by simultaneously (i) encouraging salmon to swim below the depth at which
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infestation risk is highest, and (ii) protecting any individuals that use the surface layers, for
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example, while feeding or refilling the swim bladder. In the most complete use of barrier
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technologies, fully-enclosed cages are supplied with louse-free water either filtered or
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pumped from depths below the typical depth range of copepodids (e.g. 25 m: Nilsen et al.
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2017).
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Barrier technologies (particularly skirts) are already widely used by the industry, but specific
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designs should be matched to local environmental conditions to avoid problems with low
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dissolved oxygen or net deformation (Stien et al. 2012; Frank et al. 2015; Nilsen et al. 2017).
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For example, Nilsen et al. (2017) prevented deformation of impermeable tarpaulin barriers at
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relatively sheltered sites by creating slight positive pressure within the cage (i.e. inside water
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level 2-3 cm above sea level). At more exposed sites, it is preferable to use fluid-permeable
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plankton mesh barriers (e.g. Grøntvedt et al. 2018). Brackish surface water can also reduce
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the efficacy of skirts and snorkels by causing both lice and salmon to reside below the level
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of the barrier (Oppedal et al. 2019), while there is evidence that barrier technology may
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reduce the performance of cleaner fish when used in combination (Gentry et al. 2020).
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1.2 Manipulation of swimming depth
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Salmon behaviour, primarily swimming depth, can also be manipulated in the absence of
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barrier technology to reduce spatial overlap (and therefore encounter rates) between hosts and
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parasites, especially salmon lice. Typically, the aim is to reduce encounter rates by causing
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salmon to swim below the depths at which lice are most abundant. Deep swimming
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behaviour can be promoted through the use of deep feeding and/or lighting (Hevrøy et al.
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2003; Frenzl et al. 2014; Bui et al. 2020). Where surface feeding is conducted, reducing the
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frequency or regularity of feeding (e.g. twice daily at varying times) can reduce the amount
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of time spent in the surface layers (Lyndon and Toovey 2000). Deep swimming can also be
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forced by submerging cages to the desired depth (Dempster et al. 2008; Dempster et al.
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2009), and there is evidence for reduced louse levels on salmon in submerged cages (Osland
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et al. 2001; Hevrøy et al. 2003; Sievers et al. 2018; Glaropoulos et al. 2019). Long term
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submergence can affect fish welfare as salmon lose buoyancy over time (Korsøen et al. 2009;
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Macaulay et al. 2020), however recent research indicates most welfare concerns can be
149

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
6
addressed by allowing periodic surface access or fitting a submerged air-filled dome for swim
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bladder refilling (Korsøen et al. 2012; Glaropoulos et al. 2019; Oppedal et al. In Press).
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1.3 Geographic spatiotemporal management
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A range of spatiotemporal management approaches are applied at the landscape scale to
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reduce infestation risk by controlling where and when salmon are farmed. Some farm sites
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have consistently low louse abundances and rarely require delousing (www.barentswatch.no).
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Locating farms to take advantage of beneficial oceanographic conditions and minimise
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connectivity with adjacent sites may reduce the number of host-parasite encounters over a
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grow-out cycle (Bron et al. 1993; Samsing et al. 2017; Samsing et al. 2019). Fallowing
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during periods of high propagule pressure may also delay first infestation after sea transfer of
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smolts (Bron et al. 1993).
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1.4 Filtering and trapping
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Filters and traps may be deployed in or around cages to remove infective copepodids from
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the water column before they encounter salmon. Filter-feeding shellfish racks hung around
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sea cages may reduce louse abundance if deployed at sufficient scale (Byrne et al. 2018;
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Montory et al. 2020), while powered filters are effective in the context of preventing lice and
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eggs from entering the environment during delousing (O’Donohoe and Mcdermott 2014). In
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other fish farming systems, cleaner shrimp have been used to remove parasites or parasite
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eggs from fish and nets and reduce infestation or reinfestation risk (Vaughan et al. 2018a;
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Vaughan et al. 2018b). However, this method may have limited application against sea lice
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because of the planktonic mode of dispersal and infestation (i.e. larvae do not develop within
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the cage structure). Light traps have been tested in the field with mixed results (Pahl et al.
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1999; Novales Flamarique et al. 2009), and increasing knowledge of host-locating behaviour
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in lice may present new possibilities for baiting traps with attractive chemosensory cues
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(Devine et al. 2000; Ingvarsdóttir et al. 2002; Bailey et al. 2006; Mordue and Birkett 2009;
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Fields et al. 2018). No preventative filtering or trapping methods have been widely deployed
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in the industry, but some systems have recently become commercially available (e.g.
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‘Strømmen-rør’, Fjord Miljø; ‘NS Collector’, Vard Aqua).
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1.5 Repellents and host cue masking
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Interventions may be used to repel lice or mask host cues, potentially reducing host-parasite
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encounters even when parasites enter the sea cage. Repellents or masking compounds can
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either be released into the water column or included in feed to alter the host’s semiochemical
181

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
7
profile (Hastie et al. 2013; O’Shea et al. 2017). Indeed, some existing commercially available
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functional feeds are claimed to reduce attraction of lice toward fish (e.g. Shield, Skretting;
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Robust, EWOS/Cargill). Visual cues may also be important, and the effect of modified light
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conditions on infestation rates have been trialled with mixed results. Browman et al. (2004)
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concluded that ultraviolet-A and polarisation were not important for host detection at small
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spatial scales. Light intensity interacted with salinity and host velocity to influence
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distribution of louse attachment in another study (Genna et al. 2005), while Hamoutene et al.
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(2016) reported that 24-hour darkness affected the attachment location but not abundance of
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salmon lice.
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1.6 Incapacitation
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Several methods have been proposed for disabling or killing lice—from egg to adult stages—
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in or around sea cages. These include ultrasonic cavitation (Alevy 2017; Skjelvareid et al.
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2018; Svendsen et al. 2018), direct current electricity (Bredahl 2014) and irradiation with
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short wavelength light (Barrett et al. 2020b, Barrett et al. 2020c). Some have demonstrated
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efficacy at close range (Skjelvareid et al. 2018, Barrett et al. 2020b, Barrett et al. 2020c), but
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it is currently unclear whether any such methods can be effective at commercial scale.
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1.7 Louse population control
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Interventions to suppress louse populations outside the cage environment would require
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careful consideration before deployment and must be specific to targeted louse species. Very
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little work has been done in this area, but possible avenues may include the release of
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parasites and pathogens that are specific to sea lice (Økland et al. 2014; Økland et al. 2018;
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Øvergård et al. 2018), or CRISPR-based ‘gene drives’ (McFarlane et al. 2018; Noble et al.
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2019).
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2. Reducing post-encounter infestation success
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2.1 Functional feeds
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Feeds that provide physiological benefits beyond basic nutritional requirements are termed
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functional feeds and are increasingly prevalent in industrial fish farming (Tacchi et al. 2011).
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Feed ingredients that modify the mucus layer or modulate skin immune responses may
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reduce initial attachment success or facilitate effective immune responses against newly-
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attached lice (Martin and Krol 2017). Functional feeds may also include ingredients that are
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toxic or repellent to attached lice – these are not necessarily distinct from in-feed
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chemotherapeutants, except that they tend to be derived from ‘natural’ sources (e.g. plant-
213

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sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
8
derived essential oils: Jensen et al. 2015). Functional feeds aimed at improving salmon louse
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resistance are already commercially available (e.g. Shield, Skretting; Robust, EWOS/Cargill).
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It will be important to test for any adverse effects of new functional feeds. For instance,
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glucosinolates and beta-glucans have been shown to be effective for reducing louse
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infestation (Refstie et al. 2010; Holm et al. 2016), but glucosinolates also have a range of
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effects on liver, muscle and kidney function that would need to be investigated (Skugor et al.
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2016). Hormonal treatments may also be effective at reducing louse infestation (Krasnov et
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al. 2015), but preventative hormone treatments are likely to be perceived negatively by
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consumers.
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2.2 Vaccines
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Vaccines against bacteria and viruses are increasingly widespread in fish farming. In Norway,
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antibiotics have been almost entirely replaced by injectable multi-component oil-based
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vaccines (Brudeseth et al. 2013), and there is increasing use of injected or orally administered
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vaccines in North America and Chile (Brudeseth et al. 2013). However, to our knowledge
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there is currently only one (partially effective) vaccine available for sea lice (C.
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rogercresseyi: Providean Aquatec Sea Lice, Tecnovax). While there are no in-principle
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barriers, the development of vaccines for ectoparasites is technically challenging; despite the
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identification of numerous vaccine targets in a range of ectoparasites, the cattle tick
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(Rhipicephalus microplus) remains the only ectoparasite with a highly effective vaccine
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(Stutzer et al. 2018).
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Successful development of a recombinant or DNA vaccine would allow cost-effective
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production and delivery (Raynard et al. 2002; Sommerset et al. 2005; Brudeseth et al. 2013).
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Potential vaccines exist at various stages of development, from localisation of candidate
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antigens in lice (Roper et al. 1995), demonstration of antibody production in response to
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inoculation with louse extracts (Reilly and Mulcahy 1993), and use of recombinant proteins
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to vaccinate salmon in tank trials (Carpio et al. 2011; Carpio et al. 2013; Basabe et al. 2014;
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Contreras et al. 2020). Recently, RNA interference has been used to knock down candidate
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vaccine targets and assess potential efficacy through challenge experiments (Eichner et al.
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2014; Eichner et al. 2015; Komisarczuk et al. 2017).
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2.3 Breeding for louse resistance
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Variation in louse resistance is considerable among Atlantic salmon and has a heritable
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component (Glover et al. 2005; Kolstad et al. 2005; Gjerde et al. 2011; Tsai et al. 2016;
245

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
9
Holborn et al. 2019), indicating that there is sufficient additive genetic variation for selective
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breeding. Observed variation in louse resistance is probably due to differences in expression
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of both host cues and immune responses (Holm et al. 2015). Decades of selective breeding
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has resulted in much higher growth rates for farmed salmonid strains (Gjedrem et al. 2012)
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and increased resistance to some diseases (Leeds et al. 2010; Ødegård et al. 2018; Storset et
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al. 2007; reviewed by Robinson et al. 2017). More recently, the development of high-
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throughput single nucleotide polymorphism (SNP) genotyping technology has enabled
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relatively rapid and affordable genomic selection and fine mapping of quantitative trait loci
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associated with disease resistance.
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Quantitative trait loci explaining between 6-13% of the genetic variation in sea louse
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resistance (louse density on fish) have been detected in North American and Chilean
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populations of Atlantic salmon (Rochus et al. 2018; Robledo et al. 2019). Salmon families
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with greater resistance to sea lice show upregulation of several immune pathway and pattern
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recognition genes compared to more susceptible families (Robledo et al. 2018), and the two
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major breeding companies in Norway (AquaGen and SalmoBreed) offer salmon lines that
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have been selected using marker assisted section or genomic selection for sea louse
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resistance. Use of genomic selection has been shown to increase the accuracy of selection for
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sea louse resistance by up to 22% (Tsai et al. 2016; Correa et al. 2017), and two generations
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of genomic selection focused on just sea louse resistance led to a 40-45% reduced sea louse
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infestation compared to unselected fish (Ødegård et al. 2018).
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Other possible approaches for improving sea louse resistance in Atlantic salmon include
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hybridisation of Atlantic salmon with more louse-resistant salmonid species (Fleming et al.
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2014), genetic modification of Atlantic salmon with immune genes from other salmonids, or
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use of gene editing to modify protein function or regulate the expression of genes affecting
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resistance. In the case of hybridisation or any genetic modification, the effect on other
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production traits would need to be assessed before hybrids or edited fish are used by the
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industry. Gene editing approaches have high potential (Gratacap et al. 2019), but successful
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implementation depends on knowing which genes to modify to have the desired effect, on
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developing effective methods for implementing and spreading the gene edits through the
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breeding population, and on the acceptability of the use of the technology by the general
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public and government.
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sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
10
EFFICACY OF PREVENTATIVE METHODS
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To assess the state of knowledge on the efficacy of preventative methods, we conducted a
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systematic review and meta-analysis of published studies pertaining to preventative methods.
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To find relevant studies, we searched ISI Web of Science, Scopus and Google Scholar in
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February 2020 using the following search string: (aquacult* OR farm*) AND (salmon* or
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Salmo) AND (lice OR louse OR salmonis OR Caligus). We also discovered additional studies
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referenced within articles returned by the search string. Together, our searches returned
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>1200 peer-reviewed articles, technical reports and patents relevant to lice and salmon
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aquaculture, of which 141 provided evidence on the efficacy of preventative methods and
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were included in the review.
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Studies that provided relevant response variables were included in a meta-analysis, allowing
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the comparison of effect sizes across the range of preventative approaches. For inclusion,
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studies were required to provide empirical measures of relative louse infestation densities for
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treatment groups (preventative methods used) and control groups (no preventative methods
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used). Studies that applied treatments to lice but did not directly test for effects on infestation
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were not included. Effect sizes were standardised using the natural log of the response ratio:
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lnRR = ln(µT/µC), where µT is the treatment group response and µC is the control group
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response. In most cases, response variables were either mean or median attached lice per fish.
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Where a study tested multiple qualitatively different treatments, each treatment was
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considered a replicate comparison in the meta-analysis. Where there were several
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qualitatively similar treatments (e.g. a range of doses of the same substance) the strongest
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treatment was included in the meta-analysis. Epidemiological studies typically did not have
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clear control or treatment groups; in such cases, the area or condition with the highest louse
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density was designated as the control group for the purposes of calculating a response ratio;
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this practice may inflate average effect sizes.
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A total of 41 articles provided 98 comparisons that met the criteria for inclusion in the meta-
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analysis. For each preventative approach, we calculated a median effect size. When
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calculating a median effect, weighting studies according to their sample size can reduce bias.
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However, this was difficult in practice due to inconsistent definition of units of replication
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and therefore sample size across studies. Given this, we applied weightings to studies within
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each preventative approach (except vaccination, breeding and functional feed approaches,
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which are usually challenge tested in tanks) according to the scale or level of evidence of the
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experiment (in descending order of relative weights, level A: multiple farm experiment – 1.0;
310

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sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
11
level B: experiment in full size sea cages at a single site – 0.8; level C: experiment in small
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sea cages at a single site – 0.6, level D: observational/epidemiology – 0.4; level E:
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experiment in tanks – 0.2).
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To allow a visual assessment of potential publication bias, we produced a ‘funnel plot’ in
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which study effect sizes are fitted against the precision (1/SE) of the effect. This is based on
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sample size as defined by the study authors, or else the best available approximation.
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Precision is typically increased by sample size and/or experimental power, and typically, in a
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field without publication bias, the average direction and size of effect should not vary
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systematically with study precision (Hedges et al. 1999; Nakagawa et al. 2017).
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Which preventative methods are most effective against sea lice?
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Comparison of response ratios revealed high variability in effect sizes among trials of
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preventative methods (Fig. 2), but evidence from sea cage trials indicates that barrier
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technologies can drive the largest and most consistent reductions in louse infestation levels
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(weighted median 78% reduction, range 8% increase to 99% reduction, n = 13 ; Fig. 2).
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Efficacy of specific barrier technologies appeared to be related to the extent of coverage:
325
skirts were moderately effective (median 55% reduction, range 30-81%, n = 2), snorkels were
326
highly effective (median 76% reduction, range 8% increase to 95% reduction, n = 9), and in
327
the sole closed containment study (Nilsen et al. 2017), infestations were almost entirely
328
avoided (98–99.7% reduction).
329
Approaches utilising manipulation of salmon swimming depth offered variable outcomes, but
330
with strong effects in certain situations (weighted median 26% reduction, range 72% increase
331
to 93% reduction, n = 11; Fig. 2). Geographic spatiotemporal management of farming effort
332
(or related variables such as simulated current speed: Samsing et al. 2015) had similarly
333
variable effects (weighted median 13% reduction, range 81% increase to 73% reduction, n =
334
14; Fig. 2). Functional feeds tended to have small but beneficial effects on sea louse
335
infestations (median 24% reduction, range 108% increase to 67% reduction, n = 32: Fig. 2),
336
as do published vaccine trial results (median 4% reduction, range 20% increase to 57%
337
reduction). Notably, deployment of multiple preventative methods in combination with
338
cleaner fish had highly variable effects in three published studies using replicated modern
339
commercial sea cages (weighted median 9% reduction, range 143% increase to 49%
340
reduction, n = 5: Bui et al. 2019b; Bui et al. 2020; Gentry et al. 2020).
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sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
12
Several potential preventative approaches have seen little effort to test their effects on
342
infestation rates. The use of repelling non-host cues was effective in one small-scale cage
343
study (53-74% reduction, n = 3: Hastie et al. 2013), as was filtering of copepodids using
344
oyster racks ((32% reduction: Byrne et al. 2018) or light traps (12% reduction: Pahl et al.
345
1999), and the incapacitation of lice using electric fences (78% reduction: Bredahl 2014) and
346
ultrasonic cavitation (37% increase to 39% decrease: Skjelvareid et al. 2018).
347
Efficacy of selective breeding for louse resistance should be interpreted with a long-term
348
view. Iterative improvements tend to be small-moderate but can lead to large genetic gain
349
over generations (Yanez et al. 2014; Gjedrem 2015), especially if genomic or marker assisted
350
selection for sea louse resistance is given a high weighting in the overall breeding index
351
(Ødegård et al. 2018). Estimates of heritability in louse resistance are moderate to high
352
depending on the method used (range 0.07-0.35: e.g. Gjerde et al. 2011; Glover et al. 2005;
353
Houston et al. 2014; Holborn et al. 2019), indicating that there is sufficient heritable variation
354
available for genetic improvement.
355
Is the evidence base representative and robust?
356
Most preventative approaches have only been assessed a few times. Among the 41 articles
357
that met the criteria for inclusion in the meta-analysis, 7 provided data on efficacy of barrier
358
technologies, 6 on manipulation of swimming depth, 1 on breeding, 13 on functional feeds, 2
359
on incapacitation, 2 on repellents or cue-masking, 5 on geographic spatiotemporal
360
management, 2 on trapping and filtering, and 3 on candidate vaccines. Most articles (n = 38)
361
were primarily concerned with salmon lice L. salmonis (i.e. those in Europe and North
362
America), while the remaining 3 articles targeted prevention of sea lice C. rogercresseyi (i.e.
363
those in Central or South America). All tested efficacy using Atlantic salmon.
364
Levels of evidence ranged widely: Barrier technologies had the most rigorous evidence base,
365
with multiple studies with evidence levels from A-C (Fig. 2). Evidence levels should be
366
considered when interpreting estimated efficacy, as preventative approaches may vary in their
367
scalability to commercial sea cages (e.g. viability of methods to filter or trap copepodids are
368
likely to be highly dependent on water volume).
369
Units of replication also varied widely between studies, from individual fish to tanks, sea
370
cages or farms. 51 out of 98 comparisons treated individual fish as replicates, in most cases
371
resulting in a pseudoreplicated design as individuals were kept within a comparatively small
372
number of tanks or cages (often <3 tanks or cages per group). We recommend that where
373

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sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
13
fish are treated as replicates, the number of tanks or cages should also be reported, and mixed
374
effects statistical methods employed to account for non-independence between fish held
375
within the same tank or cage (Harrison et al. 2018).
376
Finally, the meta-analysis revealed possible evidence for publication bias, with fewer studies
377
than expected present in the area of the plot corresponding to low precision and negative
378
findings (Fig. 3). In other words, the funnel plot indicates that among studies with small
379
sample sizes and/or highly variable data, those with positive results regarding efficacy of a
380
preventative method were more likely to be published. Not publishing negative findings can
381
(a) artificially inflate estimates of efficacy when averaging across studies, and (b) lead
382
researchers to waste resources testing methods that have already been found to be ineffective,
383
perhaps multiple times. Accordingly, it is important that researchers and managers are aware
384
of the potential for publication bias when considering the evidence for novel louse
385
management strategies (whether preventative or otherwise). The prevalence of publication
386
bias is likely to be influenced by the type of study and preventative method. For example,
387
tests of barrier technologies and swimming depth manipulation are generally conducted in sea
388
cages, and given the effort and cost involved, results are perhaps more likely to be published
389
in full. Other approaches may be inherently more susceptible to publication bias, for example
390
when a large range of substances or doses are tested in the early stages of a study and only
391
those that are reasonably successful are reported.
392
393
THE NEW PARADIGM: A FOCUS ON PREVENTATIVE METHODS AGAINST
394
SEA LICE
395
The evidence base demonstrates that effective implementation of preventative methods can
396
reduce infestation pressure within sea cages and therefore reduce the need for louse control.
397
A prevention-focused louse management paradigm may lead to several key benefits:
398
(1) Most preventative methods have small if any impacts on non-target organisms (like
399
mechanical and thermal delousing methods, but unlike some common chemotherapeutants:
400
Burridge et al. 2010; Taranger et al. 2015).
401
(2) Delousing treatments cause stress and injury to stock, leading to welfare concerns and
402
production losses from reduced growth, higher mortality and a lower quality product
403
(Overton et al. 2018). By focusing on avoiding encounters and reducing initial infestation
404
success, preventative methods may be targeted at infective louse stages without also
405

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
14
impacting host fish (Fig. 4). Conversely, some preventative methods can selectively target
406
host traits to improve innate resistance (Fig. 4), such as promoting parasite avoidance
407
behaviour via behavioural manipulation or immune function via functional feeds and
408
selective breeding.
409
(3) Multiple preventative methods can be deployed together and on a continuous basis,
410
although specific combinations should be trialled first (Bui et al. 2020; Gentry et al. 2020).
411
This contrasts with current louse control methods, which are less amenable to being used in
412
combination (for example, cleaner fish should not be subjected to mechanical delousing
413
along with the salmon). The technical ability already exists to place farms strategically to
414
minimise connectivity (Samsing et al. 2019), and salmon with higher louse resistance are
415
already being stocked by some farms in combination with barrier technologies (primarily
416
skirts) and/or functional feeds for louse resistance. Effective use of multiple preventative
417
methods in combination could reduce louse densities by orders of magnitude without
418
negative effects on fish welfare, although as with any control strategy, potential welfare
419
concerns (e.g. those arising from holding salmon at depth) should be tested and mitigated
420
prior to widespread deployment. Vaccines may eventually result in even greater additive
421
reductions in louse densities.
422
423
MAINTAINING LONG-TERM EFFICACY
424
Host-parasite interactions are subject to a coevolutionary arms race in which organisms must
425
constantly evolve to keep up with the coevolution occurring in opposing organisms (i.e. the
426
Red Queen hypothesis: Hamilton et al. 1990). Most lice never encounter a potential host, and
427
those that do will likely only have one opportunity to attach. This could precipitate strong
428
selective pressures, and because farmed salmon represent the majority of available hosts for
429
lice in some regions (especially in the north-east Atlantic), louse control interventions on
430
farms are likely to exert directional selection pressure on louse populations wherever certain
431
genotypes are favoured over others. Evolution of resistance occurred relatively quickly in
432
response to chemical delousing (global reviews: Aaen et al. 2015; Gallardo-Escárate et al.
433
2019) and presently remains high (Helgesen et al. 2018), although in areas where wild
434
salmonids are abundant, flow of susceptible genes from lice on wild hosts may help to
435
maintain treatment efficacy (Kreitzman et al. 2017).
436

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sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
15
It is currently unclear whether preventative methods will be similarly vulnerable to the
437
evolution of resistance in lice, but some methods will likely create suitable conditions. For
438
example, barrier technologies that span the surface layers (e.g. 0-10 m) may select for lice
439
that preferentially swim deeper. Potential for evolution will depend on many factors
440
including the heritability of the resistance to the preventative treatment in lice, the levels of
441
genetic variation existing in the louse population, the intensity of selection, treatment season,
442
frequency and geographic locations, prevailing currents and tides (louse dispersal) and the
443
biological complexity of the preventative mechanism. Nonetheless, the preventative
444
paradigm does have the advantage of a diversity of methods that may disrupt directional
445
selection for resistance to a given method. Research is needed to outline the best way
446
forward, but management strategies to slow the evolution of resistance to preventative
447
methods should heed lessons from other systems (e.g. antibiotic resistance in human
448
medicine: Raymond 2019). Potential strategies to slow the evolution of resistance to
449
preventative methods may include:
450
(1) Continuing to delouse when necessary. Effective use of preventative methods will greatly
451
reduce the required frequency of delousing, but periodic delousing will hamper the genetic
452
proliferation of any lice that successfully infest stock.
453
(2) Deployment of multiple methods in combination to counteract directional selection. For
454
example, combining skirts or snorkels with non-depth-specific methods such as functional
455
feeds or spatial management may reduce directional selection for louse swimming depth.
456
(3) Planning of spatial ‘firebreaks’ whereby farms are removed or fallowed at strategic areas
457
to minimise louse population connectivity, thus reducing reinfestation rates and potentially
458
slowing the spread of resistant genotypes between farming areas (Besnier et al. 2014;
459
Samsing et al. 2017; Samsing et al. 2019).
460
(4) Ongoing selective breeding for louse-resistant salmon lineages to ensure that genetic
461
gains are not lost through random genetic drift. Using current cohorts of wild sea lice when
462
calibrating breeding value predictions for each generation will help to ensure that genetic
463
gains continue to be relevant and account for any evolutionary developments in the louse
464
population. Like other vertebrates, salmon have a complex immune system and biology,
465
which should provide a range of potential defence options against parasites. Genomic
466
selection probably affects a number of biological processes in the fish, and sea lice would
467
therefore need to have sufficient genetic variability to be able to successfully adapt and
468

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
16
counter the genomic selection. Development of multiple louse-resistant salmon strains may
469
dampen directional selection for corresponding adaptation in louse populations.
470
Conversely, preventative methods could be utilised in a way that promotes evolution of
471
certain resistant traits (such as deeper swimming) in order to increase specificity of louse
472
populations to salmon in farming environments, and therefore reduce infestation pressure on
473
wild salmon. Modelling is needed to determine whether such an approach could prove
474
beneficial in decoupling encounters between farm-derived lice and wild salmonids.
475
476
CONCLUSIONS
477
Effective use of barrier technologies such as skirts, snorkels, or closed containment, coupled
478
with supplementary preventative methods may make delousing treatments unnecessary at
479
many sites, while high-risk locations may require additional management and regulation.
480
Breeding of louse-resistant salmon has begun; heritable variation exists, and cumulative
481
improvements are reducing susceptibility to lice in some salmon lineages. The successful
482
development of an effective vaccine would also be an important advance. In general,
483
preventative methods are preferable to reactive delousing, and moving towards a prevention-
484
focused paradigm on Atlantic salmon farms may yield significant improvements in fish
485
welfare and productivity, while avoiding significant environmental impacts.
486
487
ACKNOWLEDGMENTS
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This study was supported by the Research Council of Norway (Future Welfare project
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267800) and an Australian Research Council Future Fellowship to TD. The authors declare
490
no conflicts of interest. Members of the SALTT lab at UoM and an anonymous reviewer gave
491
valuable feedback on the manuscript.
492
493
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Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
32
TABLES
Table 1. Studies that assessed efficacy of preventative methods against louse infestation in Atlantic salmon. Effect sizes given are raw response
ratios (treatment/control group) for louse infestation densities. Smaller values indicate more effective prevention. Where a study includes
multiple treatment levels, the effect size range is given.
METHOD
EFFECT
SIZE
(T/C)
STUDY TYPE
STUDY
ENVIRONMENT
STUDY
LOCATION
FOCAL
LOUSE
NOTES
REFERENCE
1.1 Barrier technologies
Snorkel cages
0.57
Sea cage trial
Small cage
Norway
L. salmonis
Stien et al. 2016
0.05–0.37
Sea cage trial
Small cage
Norway
L. salmonis
Oppedal et al. 2017
0.17
Sea cage trial
Large cage
Norway
L. salmonis
Wright et al. 2017
0.24
Sea cage trial
Large cage
Norway
L. salmonis
Geitung et al. 2019
0.36–1.08
Sea cage trial
Small cage
Norway
L. salmonis
Oppedal et al. 2019
Skirts
0.70
Sea cage trial
Multi farm
Norway
L. salmonis
Grøntvedt et al. 2018
0.19
Sea cage trial
Large cage
Norway
L. salmonis
Stien et al. 2018
Closed containment
0.00–0.02
Sea cage trial
Multi farm
Norway
L. salmonis
Nilsen et al. 2017
1.2 Manipulation of
swimming depth
Forced submergence
0.08–1.72
Sea cage trial
Small cage
Norway
L. salmonis
Hevrøy et al. 2003
0.31–0.45
Sea cage trial
Large cage
UK
L. salmonis
Frenzl et al. 2014
1.09
Sea cage trial
Large cage
Norway
L. salmonis
Nilsson et al. 2017
0.28
Sea cage trial
Small cage
Norway
L. salmonis
Sievers et al. 2018
0.70
Sea cage trial
Small cage
Norway
L. salmonis
Glaropoulos et al. 2019
Deep lights/feeding
0.74
Sea cage trial
Large cage
UK
L. salmonis
Lyndon and Toovey 2000
1.3 Geographic
spatiotemporal
management
Location
NA
Challenge trial
Tank
UK
L. salmonis
Salinity
Genna et al. 2005)
0.45–0.93
Epidemiology
Multi farm
Chile
C.
rogercresseyi
Various risk factors
Zagmutt-Vergara et al.
2005
0.27–0.88
Epidemiology
Multi farm
Canada
L. salmonis
Spatial risk factors
Saksida et al. 2007
0.48–0.58
Epidemiology
Multi farm
Chile
C.
rogercresseyi
Spatial risk factors
Kristoffersen et al. 2013

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
33
Current speed
NA
Challenge trial
Tank
UK
L. salmonis
Genna et al. 2005
0.40–1.00
Challenge trial
Tank
Norway
L. salmonis
Samsing et al. 2015
Fallowing
NA
Epidemiology
Multi farm
UK
L. salmonis
Louse accumulation
Bron et al. 1993
1.05–1.81
Epidemiology
Multi farm
Norway
L. salmonis
Louse accumulation
Guarracino et al. 2018
Firebreaks
NA
Modelling
Multi farm
Norway
L. salmonis
Dispersal modelling
Samsing et al. 2019
1.4 Filtering and
trapping
Light traps
0.88
Sea cage trial
Small cage
USA
L. salmonis
Pahl et al. 1999
Filtering
0.68
Sea cage trial
Large cage
Canada
L. salmonis
Oyster racks
Byrne et al. 2018
1.5 Repellents and host
cue masking
In-water compounds
0.26–0.47
Sea cage trial
Small cage
UK
L. salmonis
Hastie et al. 2013
In-feed compounds
None
-
-
-
-
No published studies
Light modification
0.93–1.08
Challenge trial
Tank
Norway
L. salmonis
Browman et al. 2004
NA
Challenge trial
Tank
UK
L. salmonis
Genna et al. 2005
NA
Challenge trial
Tank
Canada
L. salmonis
Hamoutene et al. 2016
1.6 Incapacitation
Electricity
0.22
Sea cage trial
Small cage
Norway
L. salmonis
DC electric fence
Bredahl 2014
Ultrasound
0.61–1.37
Challenge trial
Tank
Norway
L. salmonis
Skjelvareid et al. 2018
Irradiation
None
-
-
-
-
No published studies
1.7 Louse population
control
Pathogens
None
-
-
-
-
No published studies
Gene drives
None
-
-
-
-
No published studies
2.1 Functional feeds
Immunomodulation
0.56
Challenge trial
Tank
UK
L. salmonis
Nucleotides
Burrells et al. 2001
0.61–1.09
Challenge trial
Tank
Canada
L. salmonis
Various additives
Covello et al. 2012
0.48–1.31
Challenge trial
Small cage
Norway
L. salmonis
Various additives
Refstie et al. 2010
0.70–0.81
Challenge trial
Tank
Canada
L. salmonis
Aquate, CpG
Poley et al. 2013
0.73–0.85
Challenge trial
Tank
Norway
L. salmonis
Various additives
Provan et al. 2013
0.84
Challenge trial
Tank
Canada
L. salmonis
CpG
Purcell et al. 2013
0.80
Challenge trial
Tank
UK
L. salmonis
Various additives
Jensen et al. 2015
0.48–0.67
Cage trial
Small cage
Norway
L. salmonis
Sex hormones
Krasnov et al. 2015
0.78
Challenge trial
Tank
Chile
C.
rogercresseyi
Various additives
Nunez-Acuna et al. 2015
0.33–0.67
Challenge trial
Tank
Canada
L. salmonis
Peptidoglycan extract
Sutherland et al. 2017
1.22
Sea cage trial
Large cage
Norway
L. salmonis
Skretting Shield (all cages
had cleaner fish)
Bui et al. 2020
2.08
Sea cage trial
Large cage
Norway
L. salmonis
Skretting Shield (all cages
Gentry et al. 2020

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
34
had cleaner fish)
Repellents/toxins
0.83
Challenge trial
Tank
Norway
L. salmonis
Phytochemicals
Holm et al. 2016
2.2 Vaccination
Recombinant protein
0.43
Challenge trial
Tank
Chile
C.
rogercresseyi
my32 protein
Carpio et al. 2011
0.45–0.47
Challenge trial
Tank
Norway
L. salmonis
my32 protein
Kumari Swain et al. 2018
0.65–1
Challenge trial
Tank
Norway
L. salmonis
P33 protein offered
strongest effect
Contreras et al. 2020
2.3 Breeding for louse
resistance
Various
0.65
Sea cage trial
Small cages
Norway
L. salmonis
Comparison of most
resistant and susceptible
families
Holm et al. 2015
Multiple methods
0.91
Sea cage trial
Multi farm
Norway
L. salmonis
All cages had cleaner fish
Bui et al. 2019b
0.51
Sea cage trial
Large cage
Norway
L. salmonis
Functional feed + deep
feeding and lighting (all
cages had cleaner fish)
Bui et al. 2020
0.79
Sea cage trial
Large cage
Norway
L. salmonis
Functional feed + deep
feeding and lighting +
skirt (all cages had
cleaner fish)
Bui et al. 2020
1.91
Sea cage trial
Large cage
Norway
L. salmonis
Functional feed + deep
feeding and lighting (all
cages had cleaner fish)
Gentry et al. 2020
2.43
Sea cage trial
Large cage
Norway
L. salmonis
Functional feed + deep
feeding and lighting +
skirt (all cages had
cleaner fish)
Gentry et al. 2020

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
35
FIGURES
Figure 1. Sea louse infestation timepoints targeted by preventative methods and delousing
treatments. Colours denote on-demand delousing (red), continuous delousing (orange) and
preventative methods (green). Line drawings indicate the stage of louse predominantly
affected by each method, L-R: larvae (nauplii and copepodids), sessile stages (chalimus I and
II), and mobile stages (pre-adults and adults).

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
36
Figure 2. Distribution of effect sizes (natural log of the response ratio: lnRR) across studies
testing preventive methods. Studies are grouped by the type of preventative method tested
(Approach). Points denote the effect size of each study, coloured by the level of evidence
provided. Negative values for lnRR indicate an effective approach. lnRR = 0 corresponds to
no difference between control and treatment groups. Boxes indicate the median and 25-75%
interquartile range of effect sizes from studies testing each approach.

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
37
Figure 3. Funnel plot of published effect sizes (natural log of the response ratio) of
preventative methods against sea louse infestations on Atlantic salmon. Effect sizes are
plotted against the precision of the experiment (inverse of the standard error). The absence of
studies on the right side of the plot is suggestive of publication bias against negative findings.
Red line indicates zero effect (lnRR = 0), orange line indicates median effect size.

Please cite as: Barrett LT, Oppedal F, Robinson N, Dempster T (In Press) Prevention not cure: a review of methods to avoid
sea lice infestations in salmon aquaculture. Reviews in Aquaculture.
38
Figure 4. Conceptual diagram outlining: (A) the current delousing treatment-dominated
paradigm for parasite control; (B) the new paradigm with a focus on prevention rather than
treatment. Red arrows indicate management actions and how they are targeted (i.e.
specificity, mediation). Blue arrows indicate supply of infective larvae (line thickness scales
with number entering cages). Black arrows indicate host and parasite traits (line thickness
scales with relative importance).