Study questions cleaner fish efficiency - Part 1

Claims that using cleaner fish to remove parasitic sea lice from farmed salmon can be economically or ethically justified are not backed up by “robust evidence” according to a new scientific report.

Farmed lumpfish are widely used by the salmon sector in countries including Norway, Scotland and the Faroes. Photo: Tom Morton

As many as 60 million cleaner fish – including ballan wrasse and lumpfish – are put into farm cages to eat lice off salmon every year, but there is limited research into how efficiently they do this job. Now scientists from the University of Melbourne, Australia, and Norway’s Institute of Marine Research (IMR) have gone through all published studies in the field - and found large knowledge gaps.

In a new review study, researchers have systematically analysed published scientific studies that have tested the effectiveness of cleaner fish.

“The increasing use of cleaner fish, and the major challenges these species face in surviving and thriving in salmon cages means that we must question whether this is appropriate use of animals. For the industry to defend their use in sea cages, their efficiency and function must be substantiated by robust evidence. Our review shows that robust evidence is still lacking,” says IMR’s Dr Frode Oppedal.

The review shows that:

• The reported effect of cleaner fish on the number of salmon lice on salmon in the different studies varied greatly.

• Only 11 published studies had examined lice predation in experimental setups with and without cleaner fish and in general replication was low,

• Almost all studies were done in small experimental cages or tanks and only one published study was performed in large, commercial-sized cages.

“Taken together, the body of evidence is not representative of today's use of cleaner fish by the industry, where up to 200,000 salmon swim in a single cage of enormous volume and depth. Here, close contact between salmon and cleaner fish is not guaranteed, as it is in small scale tanks and cages with small volumes where promising results of the effect of cleaner fish are most often recorded,” explained Professor Tim Dempster from the University of Melbourne.

The study reveals knowledge gaps that researchers believe should be filled with further research on various topics for all species used as cleaner fish.

“First and foremost, cleaner fish must be offered an environment they can thrive and survive in. The focus should be on understanding what are the best environmental conditions and optimal densities, lice removal efficiency under different environments, and breeding of cleaner fish that are better suited for life in the cages,” says Oppedal.

“The industry is gradually gaining experience with the use of cleaner fish in commercial cages, and several farms report good results from time to time. In the future, it is important that knowledge of when cleaner fish worked well, and when they did not work well, is developed and shared, and documented in scientific studies at representative scale in commercial cages” says Dempster. “An evidence-based approach will help the industry improve most rapidly without the pitfalls of mis-steps.”

Researchers believe that there is a particular need for research on the effectiveness of several wild caught wrasse species, where many millions are used each year but there are very few studies to support their lice removal effects. Lumpfish, the species most commonly used, are also the species with the best scientifically documented effect, but here too the evidence of their effects is limited to a few locations. Research should be extended to different environments and conditions. There is also a knowledge gap for how cleaner fish work together with other preventative and control measures against lice.

Improving cleaner fish efficacy

The researchers behind the study believe that more targeted, knowledge-based use of cleaner fish should increase their lice-eating effect, and lessen economic, sustainability and ethical concerns about their use.

“Increased welfare for cleaner fish will likely make them better lice-eaters, but it is also absolutely necessary for the use of cleaner fish to be able to be defended both legally and ethically,” Oppedal points out.

The study was recently published in the scientific journal Aquaculture Environment Interactions as a collaboration between researchers at the University of Melbourne and the Institute of Marine Research.

The full study, published under the title, Sea lice removal by cleaner fish in salmon aquaculture: a review of the evidence base, in Aquaculture Environment Interactions can be downloaded, for free, here.

Sea lice removal by cleaner fish in salmon  aquaculture: a review of the evidence base

ABSTRACT: Stocking cleaner fish to control sea lice infestations in Atlantic salmon farms is widespread and is viewed as a salmon welfare-friendly alternative to current delousing control treatments. The escalating demand for cleaner fish (~60 million stocked worldwide per year), coupled with evidence that they experience poor welfare and high mortality in sea cages, requires that the lice removal effect of cleaner fish be substantiated by robust evidence. Here, we systematically ana lysed (1) studies that tested the delousing efficacy of cleaner fish species in tanks or sea cages and (2) studies of spatial overlap — and therefore likely encounter rate — between cleaner fish and salmon when stocked together in sea cages. Only 11 studies compared lice removal between tanks or cages with and without cleaner fish using a replicated experimental design. Most studies had insufficient replication (1 or 2 replicates) and were conducted in small-scale tanks or cages, which does not reflect the large volume and deep cages in which they are deployed commercially. Reported efficacies varied across species and experimental scale: from a 28% increase to a 100% reduction in lice numbers when cleaner fish were used. Further, our review revealed that the interaction of cleaner fish and salmon in sea cages has rarely been documented. While much of the evidence is promising, there is a mismatch between the current evidence and the extent of use by the industry. We recommend replicated studies in 9 key areas at a full commercial scale across all species that are currently widely used. More targeted, evidence-based use of cleaner fish should increase their efficacy and help to alleviate economic, environmental, and ethical concerns.

INTRODUCTION 

Parasites are a key problem in Atlantic salmon Salmo salar aquaculture, with multiple strategies to either prevent infestations or remove pests. The industry continues to struggle with impacts arising from infestations from ectoparasitic sea lice, principally the salmon louse Lepeophtheirus salmonis and the sea louse Caligus elongatus (Costello 2006, 2009). Sea lice damage farmed stock directly by feeding on the skin, mucous, and blood of their hosts. Severe infestations can lead to skin erosion, physical damage, osmoregulatory failure, increased disease incidence, stress, and immunosuppression (Bowers et al. 2000, Grave et al. 2004, Hamre et al. 2013). Further, larvae produced by lice on farmed fish spill back to coastal waters, where they infest wild salmonids; this process has been implicated in population declines of wild stocks (Krkošek et al. 2013, Vollset et al. 2017). Accordingly, minimising sea lice infestations in farms is one of the industry’s key objectives.

Modern salmon farms typically hold hundreds of thousands to millions of fish, making effective parasite control at this scale complex. For the past 4 decades, the use of chemotherapeutants that remove salmon lice has dominated control efforts, as they are practical at this scale (Overton et al. 2019). However, reliance on chemotherapeutants has resulted in widespread evolution of resistance to most active compounds (Aaen et al. 2015). Mechanical and thermal delousing methods have been recently introduced but are stressful and lead to elevated salmon mortality rates post-treatment (Overton et al. 2019). This has prompted investment in other control methods that have minimal welfare impacts upon salmon. Among the leading contenders are invertivorous ‘cleaner fishes’ that eat attached pre-adult and adult lice stages directly off salmon (Imsland et al. 2015, Powell et al. 2018). Five main cleaner fish species are now in use: lumpfish Cyclopterus lumpus, corkwing wrasse Symphodus melops, ballan wrasse Labrus ber gylta, goldsinny wrasse Ctenolabrus rupestris, and cuckoo wrasse Labrus mixtus.

The use of cleaner fishes as biological control agents of salmon lice began in the late 1980s (Bjordal 1991, Torrissen et al. 2013). In Norway, their use in - creased rapidly from 2012, coinciding with a phaseout of chemical delousing (Overton et al. 2019). In 2018, 49 million cleaner fish were stocked in Norway, with 65% of farms using them (wrasse: 18 million; lumpfish: 31 million; Norwegian Directorate of Fisheries 2019). Similarly, in Scotland, the use of lumpfish has recently increased sharply (2016: 2 million; 2017: 6 million; Munro & Wallace 2017, 2018). In contrast, wrasse use has recently decreased (2016: 2.2 million; 2017: 58 000; Munro & Wallace 2017, 2018). In Ireland, cleaner fish use is also growing as a lice control strategy (lumpfish stocked: 2015: 105 600, 2016: 245 000; wrasse stocked: 2015: 275 800, 2016: 320 000; BoltonWarberg 2018). Cleaner fish, principally lumpfish, are also used in the Faroe Islands (Eliasen et al. 2018). 

Wrasse were first identified as potential cleaner fish via multiple experiments in tanks and cages in the 1980s and 1990s, building a foundation for industrial deployment (e.g. Bjordal 1991, Treasurer 1994, Deady et al. 1995, Tully et al. 1996). Lumpfish are a more recent addition, with the first studies to provide evidence for their efficacy at small and large commercial scale conducted in the last 5 yr, (e.g. Imsland et al. 2014a,b, 2015, 2016, 2018). Wrasse are widely used in spring and summer but become inactive at temperatures below 6°C (Imsland et al. 2014a, Powell et al. 2018). Lumpfish are better adapted to cold water, so are preferred in autumn and winter and at high latitudes (Imsland et al. 2014a, Eliasen et al. 2018). Both ballan wrasse and lumpfish are now farmed to keep up with the demand for cleaner fish in Norway. In 2018, controlled production based on wild-caught parents supplied 63% of all cleaner fish used, of which most were lumpfish (Norwegian Directorate of Fisheries 2019). 

Cleaner fish are less expensive and less stressful to salmon than chemotherapeutants (Groner et al. 2013, Imsland et al. 2018, Powell et al. 2018) and are generally more acceptable to the public than chemotherapeutant use (Imsland et al. 2018). All cleaner fish species used in salmon aquaculture are opportunistic cleaners, unlike ‘true’ cleaner fishes that have dedicated symbiotic relationships with ‘client’ fishes (Vaughan et al. 2017). In salmon cages, the expression of cleaning behaviour by wrasse and lumpfish is likely learnt and context-dependent (Vaughan et al. 2017). Once stocked in salmon cages, both wildcaught and cultured cleaners must adapt to the seacage environment and learn to approach and clean salmon. Anecdotally, salmon farmers report variable success at the commercial scale. Poor efficacy at certain places and times could be due to a range of factors. For example, access to feed pellets and biofouling may remove the need for cleaners to feed on lice and result in lower than expected lice removal rates (Imsland et al. 2015), while unsuitable environmental conditions may lead to inactivity or high mortality among cleaner fish. 

The use of cleaner fishes also raises unique ethical considerations, as measures to secure the welfare of vertebrates are typically encoded within animal welfare legislation. Concerns have arisen recently after observations of high mortalities and disease loads of cleaner fish deployed on salmon farms (Nilsen et al. 2014, Treasurer & Feledi 2014), with considerable losses due to escapes, handling, predation, or disease (Skiftesvik et al. 2014, Mo & Poppe 2018). Further, escapees of some cleaner fish (i.e. ballan wrasse: Quintela et al. 2016, corkwing wrasse: Gonzalez et al. 2016) can interact with local populations and alter their genetic structure (Faust et al. 2018). Cleaner fish can also introduce biosecurity risks for farmed salmon; for example, lumpfish are heavily parasitised by Caligus elongatus and may provide a source population for infection of farmed salmon (see Powell et al. 2018 for summary). As most wrasses used are wild-caught, high mortality rates result in continuous demand for more fish, driving fishing pressure on wrasse populations, with impacts on their ecology and population dynamics (Skiftesvik et al. 2014, Halvorsen et al. 2017). Given the evidence of poor welfare and high in-cage mortality rates, it is important that the use of cleaner fish in aquaculture is justified and guided by a strong evidence base. 

Much of the production biology and health management issues of cleaner fish have been extensively addressed in 2 previous reviews (Brooker et al. 2018, Powell et al. 2018). However, there has been no comprehensive synthesis of studies that measured how effective cleaner fish are in reducing sea lice on salmon. Here, we assessed the current evidence base for cleaner fish efficacy and encounter rates with salmon by conducting a systematic review of the literature on (1) cleaner fish lice removal efficacy, and (2) the knowledge basis about interaction levels be - tween salmon and cleaner fish in sea cages. Based on our findings, we highlight key areas that should be investigated to build a stronger evidence base re - garding cleaner fish use by industry. 

MATERIALS AND METHODS 

To discover all available literature surrounding cleaner fish use in salmon aquaculture, we searched the Web of Science and Google Scholar databases in March 2019 using the following search terms: (salmon* or aquaculture*) AND (lump* or wrasse* or cleaner*). Results were manually screened by title and abstract to identify articles or reports (‘studies’ herein) that were relevant to cleaner fish use in salmon aquaculture. For inclusion, studies needed to have addressed 1 or more of the 5 cleaner fish species currently used in salmon aquaculture. We then discovered additional studies by reading the reference lists of studies returned by the initial search. Within these search results, we conducted systematic reviews of (1) studies that assessed the delousing efficacy of cleaner fish species in tanks or sea cages; and (2) studies of spatial overlap between cleaner fish and salmon when stocked together in sea cages (and therefore likely encounter rates between the two). 

Cleaner fish efficacy 

To be included in the systematic review of efficacy, studies must have measured lice removal by cleaner fish using either a before−after or control−treatment experimental design. Where a study provided multiple control−treatment comparisons, we treated these separately (referred to as ‘comparisons’ herein). Comparisons that included 2 or more species of cleaner fish stocked together are referred to as ‘mixed’. Where multiple studies presented data from the same trials, these were combined. We recorded the experimental period, seawater temperature, type and volume of the experimental unit, degree of site exposure, details on cleaner fish stocked (species, number, and stocking density), number of salmon and their size, whether a single species of cleaner fish was present in the cage, the number of control or ‘before’ replicates, the number of treatment or ‘after’ replicates, whether the experiment was conducted at multiple study sites, and the effect size (percentage change of lice numbers by cleaner fish relative to control or ‘before’ samples). 

Spatial overlap between cleaner fish and salmon in sea cages 

To be included in the systematic review of cleaner fish behaviour and swimming depth, studies must have provided data on cleaner fish swimming depth or other relevant behaviours when stocked in sea cages with salmon. Where a study provided results from multiple distinct comparisons at different experimental scales, these were treated separately. We recorded the study period, temperature, sea cage size, degree of site exposure, cleaner fish species, number of cleaner fish stocked and the stocking density, number and size of salmon, whether more than one cleaner fish species was stocked, number of replicate cages, whether experiments were conducted at multiple study sites, whether behaviour or swimming depth was recorded, and if so, the observation method used. 

RESULTS 

The literature search returned 141 studies on the topic of cleaner fish in salmon aquaculture. Early research focused on the 4 wrasse species most commonly used in salmon aquaculture (Fig. 1). From 2003 to 2011, little research was conducted on any cleaner fish species, perhaps due to reliance on chemotherapeutants for sea lice control. Research effort increased again after 2011, coinciding with concerns around chemotherapeutants and later re - duction in their use (Aaen et al. 2015, Overton et al. 2019). However, this increase in research effort lagged behind the explosion in industrial use of cleaner fish and continues to do so. A total of 33 studies were published on cleaner fish in relation to salmon aquaculture in 2018, of which 67% concerned lumpfish, 24% wrasse, and 9% both wrasse and lumpfish (Fig. 1).

Fig. 1. Research effort over time on cleaner fish use in salmon aquaculture, measured by the number of journal articles or technical reports published in each calendar year. Bars are colour-coded by the cleaner fish species studied: black = lumpfish, white = wrasse, grey = both. Studies that tested the efficacy of cleaner fish for lice removal are also listed in chronological order (inset): (1) Bjordal (1991); (2) Treasurer (1994); (3) Tully et al. (1996); (4) Treasurer (2013); (5) Skiftesvik et al. (2013); (6) Ims - land et al. (2014a,b, 2015); (7) Leclercq et al. (2014); (8) Imsland et al. (2016); (9) Skiftesvik et al. (2017); (10) Skiftesvik et al. (2018); (11) Imsland et al. (2018). The coloured blocks indicate the species used in each study: black = lumpfish, yellow = ballan wrasse, light blue = corkwing wrasse, green = cuckoo wrasse, dark blue = goldsinny wrasse, orange = rock cook wrasse.

3.1 Cleaner fish efficacy 

Experimental tests of cleaner fish efficacy (11 studies containing 46 comparisons of lice levels with and without cleaner fish) were conducted across a broad range of experimental scales, temperatures, locations, cleaner fish species, stocking densities, and with salmon of varying sizes (Fig. 2B, in the Supplement at www. int-res. com/ articles/ suppl/ q012 p031 _ supp. pdf). The mean trial duration was 72 d (range:<1 to 335 d; Fig. 2A). Seven studies re ported water temperature, ranging from 8 to 16°C for wrasse, and 4 to 16°C for lumpfish. Aside from Tully et al. (1996) and Treasurer (2013) at a small commercial scale (2864−10 742 m3, 3 comparisons total) and Imsland et al. (2018) at a large commercial scale (37 688 m3, 3 comparisons), experimental tests of cleaner fish efficacy have been performed in tank (1 m3, 6 comparisons) and small cage (100−212 m3: 34 comparisons) scale research settings (i.e. 87% of all comparisons conducted at tank and small cage scales; Fig. 2B). Stocking densities (number of cleaner fish per salmon, %) varied widely for each experimental scale and cleaner fish species, with larger ranges observed for wrasses (tank: 5−67%; small: 4−73%; small commercial: 1−4% stocking density) compared to lumpfish (small: 5−15%; large commercial: 4−8% stocking density). Of the 10 studies that conducted experiments in sea cages, 9 provided the study location; one study was in an inner fjord (i.e. Treasurer 1994), with the remainder conducted at sites sheltered by at least one body of land. No studies were conducted at exposed coastal sites. There were 35 comparisons across 11 studies in which one species of cleaner fish was stocked within the treatment cage, allowing estimation of species-specific efficacy. Nine studies (i.e. 23 comparisons, or 50% of all comparisons) had <3 replicates. 

Comparisons reported efficacies from a 28% in - crease to a 100% reduction in lice numbers (Fig. 2B). Ninety-eight percent of all comparisons (i.e. 45 out of 46 comparisons) estimated efficacy by comparing the number of lice in cages with and without cleaner fish, with one comparison using a before− after experimental design (i.e. Bjordal 1991). One tank-based study and 2 small-scale sea cage studies stocked a single species of cleaner fish in isolation (such that the efficacy of a specific cleaner fish species could be assessed), had ≥3 replicate treatment cages, and reported a positive cleaner fish effect (tank-based: Leclercq et al. 2014; small scale: Skiftesvik et al. 2013, 2018) (Fig. 2C). One small commercial scale cage study fulfilled the same criteria, but reported a negative effect of cleaner fish, in which salmon in cages with cleaner fish had 21% more lice than cages without cleaner fish (Tully et al. 1996) (Fig. 2C). No studies examined cleaner fish efficacy at multiple sites.

Fig. 2. Relationship between the volume of the experimental unit (tanks or cages) and the measured efficacy of cleaner fish, colour-coded by (A) the duration of the study, (B) the species of cleaner fish, or (C) the species of cleaner fish, excluding studies that did not have 3 or more replicates per treatment. In C, where studies provided data for multiple treatment levels (e.g. stocking densities or cleaner fish body sizes) but did not meet the required replication within each treatment, we nonetheless included the study if taking the mean of treatment levels provided sufficient replication.

Studies reported high lice removal efficacy of ballan wrasse in experimental conditions, from tank scale (90−99% efficacy regardless of wrasse size or the presence of supplementary feeding: Leclercq et al. 2014) to small cage scale (91% efficacy: Skiftesvik et al. 2013; 49% efficacy: Skiftesvik et al. 2018) and small commercial cage scale (100% efficacy in an unreplicated comparison; Treasurer 2013). Reported lumpfish lice removal efficacies are more variable, with lower efficacies at a small scale (9−60% efficacy, but 97% for adult female lice: Imsland et al. 2014a,b; 30−40% efficacy: Imsland et al. 2016; 10% efficacy: Skiftesvik et al. 2017; 30% efficacy: Skiftesvik et al. 2018) compared to a large commercial scale (53−73% efficacy: Imsland et al. 2018). The efficacy of goldsinny wrasse has been tested at tank scale (0% efficacy: Tully et al. 1996), small cage scale (62% efficacy: Bjordal 1991; −14% efficacy: Skiftesvik et al. 2017), and small commercial cage scale (−21% efficacy: Tully et al. 1996), with highly variable effects on lice density (mean 30% reduction, range −21 to 77%). Tests of rock cook wrasse Centrolabrus exoletus efficacy at tank scale (96% efficacy: Tully et al. 1996) and small cage scale (69% efficacy: Bjordal 1991) illustrate promising lice removal effects, al though research has not been conducted in the last 2 decades or at larger scales. Bjordal (1991) tested cuckoo wrasse efficacy at small cage scale with some success, (11% stocking density: 51% efficacy; 23% stocking density: 63% efficacy), although the authors reported that the wrasse did not become effective until after a delousing treatment. Finally, the efficacy of corkwing wrasse has been tested in 2 small cage scale studies, with mixed ef fects (−28% efficacy: Skiftesvik et al. 2017; 58% efficacy: Skiftesvik et al. 2018).

3.2. Spatial overlap between cleaner fish and salmon in sea cages

The literature search revealed several studies on cleaner fish behaviour when stocked with salmon, but it remains difficult to assess spatial overlap and likely encounter rates between cleaner fish and salmon in commercial settings. One study (Tully et al. 1996) recorded cleaner fish and salmon swimming depths simultaneously, via SCUBA diving observations (Table 1). However, the authors did not observe any cleaning behaviour during SCUBA diving observations between October and December and re - ported that goldsinny spent most of their time swimming close to the net and consuming biofouling orga nisms (Tully et al. 1996). A large proportion of wrasse was also observed resting in a torpid state during November−December (Tully et al. 1996). 

Stocking densities varied for lumpfish (small: 4.7−40% stocking density; large commercial: 6% stocking density) and wrasse (small: 4.7−10% stocking density; small commercial: 0.3−7% stocking density; Table 1). Of the 7 studies and 25 comparisons conducted, 17 comparisons were conducted with one species of cleaner fish within the treatment cage (T able 1). Four studies (i.e. 15 comparisons) had ≥3 replicates. Seven comparisons monitored cleaner fish behaviour and swimming depths within small commercial-scale sea cages, but salmon swimming depths were only recorded in one. Salmon swimming depth was not monitored in any of the small-scale studies. Further, no studies were conducted at a large commercial scale or across multiple study sites.