REVIEW

Sustainable production and use of

cleaner fish for the biological control
of sea lice: recent advances and
current challenges
Adam J Brooker,1 Athina Papadopoulou,1 Carolina Gutierrez,2 Sonia Rey,1 Andrew Davie,1 Herve Migaud1

Currently, cleaner ish are one of the most widely used sea lice control strategies in Atlantic salmon aquaculture.
Two species are currently being farmed in North Atlantic countries, ballan wrasse (Labrus bergylta) and lumpish
(Cyclopterus lumpus), and the sector in most countries is rapidly expanding towards self-suiciency. The species
are very diferent both in terms of their biology and life histories and, consequently, production and husbandry
methods must be tailored to each species. There are numerous health challenges currently experienced in both
species, with bacterial and parasitic diseases being the most prevalent, and cohabitation with salmon may
increase the risk of disease. Good husbandry and routine health monitoring are essential, although treatment
is oten required when disease outbreaks occur. Ballan wrasse and lumpish are both proven to be efective
salmon delousers, although delousing eicacy can be variable in farmed ish; the provision of suitable habitat
and acclimation to net-pen conditions may encourage natural behaviours, including delousing, and the use of
operational welfare indicators can highlight potential welfare issues. Cleaner ish research is progressing rapidly,
although much of the basic knowledge regarding the species’ biology remains unknown. The simultaneous
domestication of two new marine aquaculture species is a signiicant challenge demanding sustained efort and
funding over a prolonged period of time. Research must focus on enhancing the robustness of the farmed stocks
and increasing hatchery outputs to meet the urgent demands from the salmon sector and protect wild stocks from
overishing.

Introduction the production losses, Abolofia et al4 estimated that

The greatest disease challenge currently limiting sea lice infection typically results in up to a 16 per cent
production within the global Atlantic salmon industry reduction in production biomass, which translates
is infection by caligid sea lice. Along with causing approximately to a 9 per cent loss in farm revenues.
significant physical and biochemical damage, including Driven by environmental and welfare concerns, and
skin lesions, loss of protective skin function leading to economic pressures, many new innovative strategies
risk of secondary infections, osmoregulatory imbalance, for pest control in salmon farming have been developed
immunosuppression and increased stress,1 2 there are over recent years, including lice removal technologies
significant economic impacts due to production losses using brushes or water jets (eg, hydrolicer), novel bath
and treatment costs. The global economic impact of sea treatments using warm water (thermolicer) or fresh
lice was estimated at £700 million in 2015, with costs water, physical barrier technologies (eg, snorkel cages
likely to have continued to rise since then.3 In terms of and lice skirts), light regimes to manipulate salmon
swimming behaviour and passive lice control using
laser technology (Stingray, Stingray Marine Solutions)
Veterinary Record (2018) doi: 10.1136/vr.104966 (reviewed in Holan et al).5 Other methods are in
1
development, including new chemotherapeutants,
Institute of Aquaculture, University of Provenance and peer review Not
vaccines, feed additives and selective breeding. Since
Stirling, Stirling, UK commissioned; externally peer
2
Marine Harvest Scotland Ltd, Fort reviewed. 2010, one of the most widely adopted alternative pest
William, UK control strategies is the use of cleaner fish as a biological
Received April 5, 2018 control. While not a novel method with the first proof-of-
E-mail for correspondence: Institute
Revised June 26, 2018 principle reported in the early 1990s,6 7 the expansion of
of Aquaculture, University of Stirling,
Accepted July 6, 2018
Stirling FK9 4LA, UK; [email protected] farmed cleaner fish production has led to the emergence

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 20427670, 2018, 12, Downloaded from https://bvajournals.onlinelibrary.wiley.com/doi/10.1136/vr.104966 by BINGOL UNIVERSITY, Wiley Online Library on [12/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
of a new sector with new production challenges, This paper provides a comparative overview of the
including the health and welfare management of these scientiic knowledge and industry practices regarding
new aquaculture species. the biology and deployment of cleaner ish with an
Before circa 2011, all cleaner ish deployed in emphasis on the health challenges and welfare of both
salmon sea cages were wild-caught wrasse species species.
from the family Labridae, including cuckoo (Labrus
mixtus), ballan (Labrus bergylta), corkwing (Symphodus Overview of cleaner ish production
melops), goldsinny (Ctenolabrus rupestris) and rockcook Although being used for a common purpose, ballan
(Centrolabrus exoletus). Based on farm experience, wrasse and lumpfish are quite distinct, both in terms
there was a preference towards the deployment of their biology, ecology and life histories (table 1). This
of ballan, goldsinny and corkwing wrasse, driven can be beneficial as each species can be used for sea lice
primarily by stock availability8 and enhanced delousing control under different conditions, with each having its
performance.9 10 The level of exploitation in Norway own biological niche in the net-pen environment, but
(where the longest record of catch and deployment it also means that production and husbandry methods
exists) provides an insight into the scale of application, must be tailored to each species.
where the use of wild wrasse increased from 1.7 million Ballan wrasse are protogynous hermaphrodites18 19
ish in 2008 to 20 million in 2016.11 However, such with a complex hierarchy and a highly skewed sex ratio,
increasing demands for cleaner ish due to the recent which makes broodstock management challenging.20
industry expansion together with increasing sea lice The spawning window is naturally in April–June,21 but
pressures and biosecurity concerns, has led to the this can be extended in captivity using environmental
farming of cleaner ish to control the quality and health manipulation.13 Due to their long generation time
of deployed animals and ensure the environmental (reaching puberty at ~6 years for females and 12 years
sustainability of this pest management strategy. To this for males19), current hatchery production is exclusively
end, two species are currently being farmed in North from wild-caught broodstock, although F1 stocks are
Atlantic countries (UK, Ireland, Norway, Iceland and now being retained by commercial hatcheries to act
Faroe Islands),12 ballan wrasse (reviewed in Davie et as future potential broodstock. Ballan wrasse typically
al.13 and Lekva and Grotan14) and lumpish (Cyclopterus require 18 months to reach their deployment size of
lumpus) (reviewed in Powell et al).15 Despite farming 40–50 g,22 which includes a two-month live feeds period
being in its infancy with the irst farmed ballan wrasse with weaning to formulated feeds being completed by
deployed in salmon pens in 2013 in Scotland,16 the about 70–90 days posthatch depending on hatchery
sector in most countries is rapidly expanding towards protocols (igure 1). Research is ongoing to optimise
self-suiciency. In Norway, 17.2 million (46 per cent) the species’ growth potential primarily through
of the 37.4 million cleaner ish deployed in 2016 were environmental and nutritional manipulations with
of farmed origin, comprising 15.9 million lumpish and the objective being to shorten the production period to
1.3 million ballan wrasse.11 In comparison, UK farmed reduce costs, optimise the use of hatchery and nursery
cleaner ish production in 2016 was 1.9 million lumpish facilities and increase overall productivity. The primary
and 118,000 ballan wrasse, which was 68 per cent focus is on improving understanding of nutritional
of the total cleaner ish deployed.17 Annually, these requirements and digestive physiology, especially
numbers are increasing signiicantly, primarily driven given their agastric digestive system.23 As in most other
by lumpish production as they are proving to be the non-domesticated marine ish species, larviculture
least challenging in terms of hatchery production. can be challenging with high mortalities during the

Table 1 Natural range, population dynamics and reproductive traits in wild ballan wrasse and lumpfish
Ballan wrasse Lumpfish
Natural range East-Atlantic coasts (Morocco— Trondheim and Iceland).18 Widely distributed in North Atlantic (Hudson Bay—Bermuda, Greenland,
Iceland—Iberian Peninsula).106
Natural habitat Rocky reefs.18 Bentho-pelagic.107
Home range High site fidelity.41 45 Extensive migrations between feeding and breeding grounds.47 108
Status of wild stocks Least concern on IUCN Red List,109
although not assessed since 2010. Near threatened on the IUCN Red List.110 Decrease in some spawning stocks in
recent decades, may be overexploited.111
Population genetics Two predominant genetic clades (Scandinavian and Celtic) based on Three distinct populations based on microsatellite markers: Maine-Canada-
mitochondrial haplotypes.112 Greenland, Iceland-Norway and Baltic Sea.111
Gender system Protogynous hermaphroditic resulting in highly skewed sex ratio.19 113 Gonochoristic.114
Natural diet and Omnivorous, primarily hard-shelled crustaceans, eg, decapods, isopods and Larger planktonic organisms (harpaticoids, amphipods, isopods). Sea lice
digestive system molluscs19; substrate grazers.9 Agastric digestive system.23 regularly ingested.48 107 115 Stomach present.
Fecundity 105–154 eggs/g per season in 650–950 g fish21; ~100 eggs/g per spawning Wild Greenland lumpfish potential fecundity of 49–60 eggs/g for 2 kg fish,
in 500 g fish.116 increasing with latitude,117 and mean of 61 eggs/g for 2 kg fish from Gulf of St
Lawrence.118
IUCN, International Union for Conservation of Nature.

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 20427670, 2018, 12, Downloaded from https://bvajournals.onlinelibrary.wiley.com/doi/10.1136/vr.104966 by BINGOL UNIVERSITY, Wiley Online Library on [12/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Figure 1 Typical commercial production timelines for ballan wrasse and lumpfish. DD, degree days, DPH, days posthatch. Image credits: AJ Brooker,
C Gutiérrez, A Chalaris, T Cavrois, JC Navarro.

early larval stages, primarily during irst feeding and unknown whether they predate sea lice on salmon
weaning. There are also anecdotal reports of deformities or other hosts in the wild. The natural diet of the
in juveniles, primarily jaw and spinal pathologies, two species is quite distinct and reflective of their
which could reduce their delousing eicacy. However, different environmental preferences (table 1). Cleaner
there remains no clear data, nor has the aetiology for fish mutualism is widely recognised in tropical-reef-
such conditions been identiied, although, as with other dwelling wrasse,31 32 so cleaning behaviour may
marine species, it is most likely multifactorial. be innate, in the Labridae at least. In tank studies,
Farmed lumpish are currently produced from wild- farmed ballan wrasse naïve to both salmon and sea
caught broodstock, which are culled and the gametes lice reduced sea lice prevalence from 12 to less than
stripped for artiicial fertilisation.24 Due to the increased 0.5 adult lice per salmon after 60 hours even when
biosecurity risk associated with wild broodstock, a supplementary food (crushed mussels) was available.28
postmortem health screening is recommended, and Furthermore, Skiftesvik et al33 found that farmed
only egg masses from clean parents should be used for wrasse were as effective as wild wrasse at delousing
production. Natural spawning in captivity is possible,25 in cage studies. Imsland et al34 reported that lumpfish
although quality is generally poorer than in egg masses in experimental net pens maintained sea lice levels
produced using artiicial fertilisation.15 Given the well- significantly lower than in controls, although there was
established supply chains for mature adults from caviar evidence of variable performance that may be related to
isheries,26 wild ish remain the favoured source of genetics or animal size. All studies have found that both
broodstock. The production cycle for lumpish is nearly species preferentially predate larger, motile lice stages,
60 per cent shorter (ive to seven months to a deployment although chalimus stages can also be predated.35
size of around 20 g) than in ballan wrasse (igure 1), Lumpish are deployed at a smaller size than ballan
which is one of the main drivers for the increased focus wrasse (15–30 g vs 40–50 g) as their broader cross-
on the production of this species in Ireland, UK, Norway, section prevents their escape from net pens at these sizes
Faroes, Iceland and Canada. The rapid growth rate (table 2). Small lumpish (20–30 g) are thought to be
of lumpish (SGR 1.5 per cent–3.5 per cent per day27) more efective delousers than larger lumpish (>75 g),36
brings with it challenges in production management, but more research is required to conirm this. Conversely,
primarily due to a conlict between ensuring efective delousing was found to be more rapid in larger ballan
vaccination strategies while maintaining size grades wrasse (~75 g) than smaller ish (~23 g), although there
desired for deployment. However, it is anticipated that is an increased risk of aggressive behaviour leading to
closed life cycle management will be viable given the salmon injuries when deploying larger wrasse during
species’ short generation time,15 which should enable the irst year of seawater production.28
the selective improvement of traits of interest (eg, slower Stocking rates are generally higher for lumpish
growth, enhanced delousing and disease resistance). than for ballan wrasse. Treasurer,37 Skitesvik et al33
and Leclercq et al28 recommended a stocking ratio of
Cage management: cleaner ish behaviour, welfare and 5 per cent wrasse:salmon, whereas Imsland et al30 34 38
reuse used stocking ratios of 10 per cent and 15 per cent for
Behaviour and delousing eiciency lumpish. Anecdotal evidence from the Scottish and
Ballan wrasse and lumpfish are omnivorous, Norwegian salmon industries indicate that stocking
opportunistic feeders and they are both proven to be ratios of approximately 5 per cent for ballan wrasse and
effective salmon delousers.28–30 However, it remains 8 per cent–10 per cent for lumpish are widely used.

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 20427670, 2018, 12, Downloaded from https://bvajournals.onlinelibrary.wiley.com/doi/10.1136/vr.104966 by BINGOL UNIVERSITY, Wiley Online Library on [12/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Table 2 Comparison of deployment and husbandry practices for farmed ballan wrasse and lumpfish in salmon sea pens (with a focus on UK production)
Ballan wrasse Lumpfish
Deployment window Spring/summer with increasing water temperature. Late autumn/winter with decreasing water temperature.
Transportation Fish starved 24 hours prior transport via road in tanks with hides present, then Fish starved 24 hours before transport via road in tanks with hides present,
secondary transport via boat to net-pen site. then secondary transport via boat to net-pen site. High-stress periods are
loading, handling, secondary transport.119
Deployment size At least 40–50 g to prevent escape through net mesh.37 Larger wrasse may be Typically 15–30 g119 (R Hawkins, Marine Harvest Scotland, personal
more effective delousers.28 communication, 2017). Ineffective delousers when mature (400–500 g,
14–16 months38).
Stocking rate 5% of salmon number.28 33 37 10% of salmon number.30 34 38
Use of hides and substrates Plastic fake kelp; various configurations available commercially, eg, curtain, Plastic fake kelp and smooth, flat surfaces for resting; various configurations
lantern, float frame. available commercially.
Feeding behaviour Will not feed below 6°C, winter dormancy.40 120 121 Will feed as low as 4°C.27
Swimming activity Slower than lumpfish, prefers edges and corners.43 Higher activity rates than ballan wrasse. Covers whole pen area.43 Active
foraging during day, aggregate on smooth surfaces at night.42
Buoyancy Physoclistic; rapid pressure changes should be avoided.122 123 Observations of No swim bladder, but near-neutral buoyancy due to cartilaginous skeleton,
swim bladder overinflation in hatcheries and net pens. extensive subcutaneous jelly and loose-fibred muscles.124
Recapture Unbaited creels are commonly used to sample or recapture. Hides or habituation to feeding sites are preferred.

Strict biofouling control and salmon mortality small home ranges and limited migrations.45 They are
removal is important when using ballan wrasse, diurnally active and nocturnally quiescent, sheltering
as these alternative food sources can preclude overnight in rocky crevices.41 45 46 Wild lumpfish have an
delousing.9 33 These practices are considered less offshore, semi-pelagic lifestyle and are often associated
important for lumpish, which may beneit from the with floating seaweed.47–49
alternative food sources,29 and indeed, the Faroese Despite their diferent lifestyles, the habitat
aquaculture industry promotes net biofouling to reduce requirements of both ballan wrasse and lumpish can
the efects of strong coastal currents in the net pens.39 be met through the use of artiicial substrates, or hides
Water temperature is an important consideration (table 2). These provide shelter for ballan wrasse,
for both ballan wrasse and lumpish as it dictates their particularly during the night, although the net-pen
deployment windows. The ballan wrasse is a temperate corners and sides are preferred locations for ballan
species and tends to have slower swimming and foraging wrasse at any time of the day or night.43 Imsland et al38
activity at temperatures below 10°C40, and below 6°C found that while lumpish spent much of the daytime
they enter into a state of torpor41 (table 2). In contrast, foraging, they were usually found resting within or
lumpish continue to feed at 4°C,27 but industry reports under loating weed when not feeding, and at night
suggest that they prefer lower temperatures and are they tended to aggregate on smooth substrates using
more prone to disease at higher temperatures (>10°C). their abdominal suckers.42 Various hide conigurations
Consequently, wrasse are best deployed in the spring/ are produced commercially, but they are typically
summer when water temperatures are rising, while made from strips of plastic attached to ropes to form
lumpish are best deployed in the autumn/winter when strands of artiicial kelp with the addition of rigid
water temperatures are dropping (table 2). plastic substrates for lumpish to adhere to.42 Continued
Ballan wrasse and lumpish are diurnal species; they research into hide types, colours and locations in the
are active during the day, when they are likely to exhibit net pen may yield further enhancements.
delousing behaviour, and rest at night.41–43 Lumpish Sea lice levels in commercial salmon net pens are
tend to swim at shallower depths than ballan wrasse, maintained as low as possible. In the UK, for example,
which adjusted their swimming depth according to the the Aquaculture and Fisheries (Scotland) Act 2007 sets
time of day in commercial net-pen trials43 (table 2). The a treatment threshold of 0.5–1 adult female lice per
species’ diferences in temperature preferences and ish. These low lice levels are inadequate to sustain a
behaviour suggest that a combined wrasse/lumpish population of cleaner ish, and although both wrasse
deployment strategy may prove to be more efective and lumpish are known to graze on biofouling in
than a single-species approach. net pens,9 29 30 supplementary feeding is essential to
maintain the condition and welfare of the cleaner
Husbandry practices ish.33 50 Several feed manufacturers now produce
Good health and welfare can be promoted through good pelleted diets for ballan wrasse and lumpish, and these
husbandry practices, and while many improvements can be delivered by hand or automatic feeders into
in cleaner-fish husbandry have already been made, the hides or near the pen edges, which allows feeding
including transportation, acclimation, supplementary behaviour to be monitored. Typical feeding rates are
feeding, hides and substrates, many more will come as 2 per cent of the ish biomass every other day.44 As
new knowledge becomes available.44 In the wild, ballan ballan wrasse are predominantly substrate grazers,
wrasse inhabit coastal reefs, preferring the cover of their condition can be better maintained using agar-
rocks or kelp19 and tend to be territorial with relatively based feed blocks placed within small feeder shelters

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 20427670, 2018, 12, Downloaded from https://bvajournals.onlinelibrary.wiley.com/doi/10.1136/vr.104966 by BINGOL UNIVERSITY, Wiley Online Library on [12/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
away from the main hides.50 The use of this water-stable techniques could involve sonar or acoustic tagging of
feed is becoming more widespread and has also being sentinel cleaner ish.43
trialled for lumpish.51
The acclimation of hatchery reared cleaner ish Reuse and end use
to the net-pen conditions is likely to be beneicial in Cleaner fish trained in salmon delousing are a valuable
reducing stress and encouraging natural behaviours resource, and once a production cycle is finished,
(including delousing). For example, retaining ballan the capture and redeployment or breeding of these
wrasse in a small conditioning pen containing hides fish could be considered to be an efficient use of this
and agar feed within the main net pen for several resource. However, biosecurity issues may prevent their
weeks before release has been reported to improve reuse, and this practice may not be permitted in some
deployment success.44 countries. While reuse may be an option for wrasse, the
rapid growth rates of lumpfish and their tendency to be
Welfare poor delousers and aggressive when mature36 precludes
As cleaner fish are produced for their delousing their reuse.
behaviour as a pest management strategy rather than For cleaner ish that can no longer be used as
any physical characteristics, good welfare is essential to delousers there are several possibilities for their end
promote their natural behaviours. For any new species use if they are harvested appropriately. As availability
in aquaculture, it is important to develop indicators to increases, there is increasing interest from the retail
define and monitor welfare. sector for both species, including the use of ballan wrasse
The development and standardisation of best for sashimi (Cornwall Good Seafood Guide63); there is
management practices (eg, RSPCA cleaner ish welfare an emerging market for whole and illeted lumpish,
standards52) and routine health checks are essential to especially in Asia, and exports to China bring in more
minimise disease and maintain a good welfare status. than €18 million per year to the Icelandic economy.64
To monitor health and welfare both in hatcheries and However, further research is required to develop this
following deployment at sea, operational welfare market, and public perception may be an issue due to
indicators (OWI) must be deined for each cleaner its unusual appearance.65 A further market opportunity
ish species, and these should be based on preferred for lumpish could be the production of lumpish roe
environmental conditions, physical and physiological from mature captive females as a sustainable alternative
status or behaviour.53 Mortalities are a deinitive to wild isheries,26 although this would require the
indicator of poor health and welfare, and they should development of additional rearing facilities to ongrow
be recorded along with condition and growth rates. the ish once they had exceeded their efective delousing
Fulton’s condition index54 55 can be used for both size. Finally, biliverdin, a compound responsible for the
species to indicate general animal condition. However, blue coloration of ballan wrasse and lumpish66 has
it should be noted that given their rotund body form, several potential applications in research, medicine
the typical ranges recorded for lumpish (eg, 4–4.538 are and biotechnology, including luorescence microscopy
much higher than in most other teleosts. Nonetheless, and as a storage medium for transplant organs. While
datasets have conirmed that the species follows an large quantities could potentially be extracted from
isometric growth pattern so the method is valid56 cultured ballan wrasse blood,67 the cost of extraction
(A Davie, unpublished data). compared with other sources must be further studied.
In many ish species, in damage can be a result of
aggression and a sign of stress,57 and these injuries Health challenges, prevalence and management
can be a portal for bacterial and fungal infections. Fin Primary diseases during production
damage indices have been developed for both wrasse58 There are numerous health challenges currently
and lumpish (S Rey, unpublished data) and could experienced in both farmed ballan wrasse and lumpfish,
easily be implemented as a physical OWI. Elevated and this is a top priority area for research.
blood glucose and lactate is a sign of stress and can be
measured using handheld meters, and this method has Bacterial diseases
been validated for ballan wrasse.59 Other physiological Bacterial diseases are currently the primary challenge
parameters could be used (eg, hepatosomatic index60 in both species. Secondary bacterial infections by
or liver-colour scoring index39), although they require opportunistic pathogens may be triggered by poor
sacriicial sampling. Behaviour can also be used to husbandry or water quality in the hatchery/nursery,
assess animal welfare.61 62 Environmental, dietary and handling during vaccination, nutritional imbalance,
social preferences can be determined by choice tests stress or cannibalism (common in early stage lumpfish
or place preference tests, and routine monitoring of in hatcheries).48
behaviour at salmon farms may be achieved by visually Atypical strains of the bacterium Aeromonas
observing and recording behaviour at the surface or salmonicida are the aetiological agent of atypical
underwater using video cameras, or more quantitative furunculosis, afecting both ballan wrasse and lumpish

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 20427670, 2018, 12, Downloaded from https://bvajournals.onlinelibrary.wiley.com/doi/10.1136/vr.104966 by BINGOL UNIVERSITY, Wiley Online Library on [12/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Figure 2 Clinical signs of bacterial and parasitic diseases in lumpfish and ballan wrasse: (A) external ulcer indicative of atypical Aeromonas salmonicida
in lumpfish; (B) multifocal granulomas in lumpfish kidney characteristic of atypical A salmonicida; (C) external ulcer indicative of atypical A salmonicida
in ballan wrasse; (D) multifocal granulomas in ballan wrasse liver characteristic of atypical A salmonicida; (E) decoloration and enlargement of the caudal
peduncle symptomatic of Vibrio species in lumpfish; (F) skin lesions as white patches around the eyes symptomatic of Pasteurella species in lumpfish; (H)
amoebic gill disease in ballan wrasse resulting in pale plaques on the gills and (G) amoebic gill disease in lumpfish resulting in pale plaques on the gills. Image
credits: C Gutiérrez, L Sheriff, G Ramírez-Paredes.

when water temperatures exceed 13°C.68 It is the most Pasteurella species and other pathogens, such
frequent cause of bacterial disease outbreaks in both as Pseudomonas anguilliseptica, Tenacibaculum
species resulting in considerable economic losses as maritimum, Moritella viscosa and Piscirickettsia
a commercial vaccine is not currently available. The salmonis, have been reported as primary pathogens
bacterium is classiied into subtypes (A-layer types) causing pasteurellosis in lumpish.74–82 Symptoms of
by the virulence array protein gene, vapA. Ballan Pasteurella infections commonly include skin lesions
wrasse are more susceptible to subtype V in Scotland as white patches around the eyes, tail rot and bleeding
and both V and VI in Norway, while lumpish appear in the gills, the base of the ins and tail80 (igure 2F),
to be susceptible only to subtype VI.69 70 Outbreaks although similar symptoms have been observed in other
have occurred in hatcheries and at cage sites, although bacterial infections, for example, skin ulcers and tail rot
asymptomatic ish can also be positive. Disease in T maritimum infections in lumpish in Norway.81
progression is chronic, and high mortalities have been In Norway, epitheliocystis has also been observed
recorded.68 Afected ish show external ulcers on the skin in ballan wrasse, which is an intracellular bacterial
and ins, granulomas in the internal organs and luid disease caused by Candidatus species Similichlamydia
accumulation in the abdominal region (igure 2A–D). labri. nov. and afects the secondary lamellae of the
Vibriosis in cleaner ish is caused by Vibrio gills.83
anguillarum, V ordalii and V splendidus. Pathology is
similar for both species with external lesions (ulcers, Parasitic diseases
oedema and haemorrhages), enlargement of the caudal The ubiquitous Neoparamoeba perurans, the
peduncle due to luid retention and necrosis of internal causative agent of Amoebic Gill Disease (AGD), has
organs (igure 2E). While lumpish are susceptible to both been reported as a natural infection in both ballan
species, only V anguillarum has been isolated from wild wrasse and lumpfish, and experimental infection has
ballan wrasse to date, with up to 60 per cent mortality been successful in lumpfish cohabiting with infected
in 50 g ish injected with the bacterium.71 72 Other Vibrio salmon.84 Primary histopathology shows pale patches
species have been isolated from cleaner ish but their at the bases of gill filaments, hyperplasia of epithelial
pathogenicity is unclear.70 Birkbeck and Treasurer73 cells and fusion of gill lamellae84 85 (figure 2G,H).
demonstrated that V splendidus and V ichthyoenteri are Low-to-moderate mortalities in hatcheries and cage
part of the natural microbiota of wrasse, and hence, sites have been reported due to AGD.
Vibrio species may be opportunistic, causing disease The microsporidian Nucleospora cyclopteri has been
only if the immune system is suppressed. reported in wild lumpish with 25 per cent of ish showing

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 20427670, 2018, 12, Downloaded from https://bvajournals.onlinelibrary.wiley.com/doi/10.1136/vr.104966 by BINGOL UNIVERSITY, Wiley Online Library on [12/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
chronic clinical signs, such as pale and uniformly bronopol, formalin and even itraconazole have not
enlarged kidneys (renomegaly), exophthalmia and been 100 per cent successful.
skin lesions.86 Horizontal transmission is conirmed,
although vertical transmission may also occur due Prevalence and management
to the close association of spores with eggs. All wild Prevalence
lumpish used as broodstock for commercial production Bacterial diseases may lead to mass mortality,
must be tested for N. cyclopteri as there is no efective especially in the lumpfish. A survey conducted in
treatment available. Reports on farmed Norwegian Norway in 2013 reported 48 per cent mortality among
lumpish, have found coinfections of N. cyclopteri and the stocked cleaner fish population, with 75 per cent
Kudoa islandica.87 The microsporidian Tetramicra caused by bacterial infections.71 Similar findings were
breviilum has recently been reported in lumpish reported in autumn/late summer 2015, when bacterial
broodstock causing lethargy, anorexia, exophthalmia, agents were confirmed in nearly 80 per cent of case
severe bloating like ascites, vacuolisation and white materials, and atypical furunculosis and vibriosis
nodules in most of the internal organs, while skeletal were the most common causes of mortality in cleaner
muscle liquefaction and microsporian xenomas were fish.95
observed in the skin, internal organs, gills and eyes.88 AGD is prevalent in hatcheries where water quality is
Other ciliates, such as Trichodina species and poor and sand-iltered water is not used (low-through
Uronema-like species, have been reported as incidental hatcheries) or when recirculation systems are topped
indings on the skin or gills of lumpish. Heavy infections up. Some evidence suggests that UV irradiation or
may lead to mortalities if unattended.15 ozonisation is inadequate to kill free-living amoeba,
and in some cases amoeba-forming pseudocysts can
Viral diseases pass through the system and be re-activated.96
Viral haemorrhagic septicaemia (VHS) is a notifiable
disease in Scotland and has been reported in wild- Management
caught cleaner fish from Shetland.89–91 It has not Following deployment, the survival of cleaner fish is
been found in farmed ballan wrasse, but was isolated often poor in net pens cohabiting with Atlantic salmon,
in Icelandic lumpfish for the first time in 2015.92 and there are concerns regarding the welfare of wild
Interestingly, lumpfish infected with VHS were more and farmed cleaner fish.97 Good husbandry, such as
susceptible to the infectious pancreatic necrosis (IPN) the provision of hides, clean nets and supplementary
virus (another notifiable disease) during experimental feeding,50 and routine health monitoring are essential.
infections.75 AGD can be controlled using hydrogen peroxide,
In a recent cardiomyopathy syndrome (CMS) event which signiicantly reduces the numbers of
at a salmon farm in Ireland, ballan wrasse tested amoebae present in the gills (C Gutiérrez, personal
positive for low levels of piscine myocarditis virus communication). In Atlantic salmon, freshwater
(PMCV).93 Only small numbers of ish were tested and bathing signiicantly reduces the presence of amoebae
the histopathology was inconclusive. However, ballan and mucoid patches on gills98; the treatment is efective
wrasse are known to be susceptible to the virus and can for lumpish and is used where possible,99 but it is
be potential carriers. not used for ballan wrasse due to their low freshwater
A recently discovered lumpish lavivirus (family tolerance. Freshwater is preferred to hydrogen peroxide
Flavoviridae) has been associated with moderate-to- as clearance rates are higher, and hydrogen peroxide
high mortality in farmed lumpish in Norway with the can cause mortalities if gills are compromised (CG,
virus present in most tissues but elevated in liver and pers. obs.). In hatchery trials, 15 ppt brackish water
kidney, although it has also been detected in lumpish over three days achieved 100 per cent clearance of
with no clinical signs.94 Clinical signs are anaemia, pale AGD in ballan wrasse (P. Featherstone, Marine Harvest
gills, liver inlammation and necrosis and inlammation Scotland, personal communication, 2017), although
of the abdomen, and it is recommended that all wild- further investigation of this treatment for wrasse in sea
caught lumpish broodstock are tested for the pathogen pens is required.
using RT-PCR, with monitoring and regular screening Authorised antimicrobial treatments (eg,
during the production cycle.94 oxytetracycline or lorfenicol) are used in net pens to
control clinical outbreaks when required. While broad-
Fungal diseases spectrum antibiotics are efective against most bacteria,
Systemic fungal infections in adult lumpfish by signiicantly improving survival rates, some bacterial
Exophiala species have been reported from marine diseases, such as pasteurellosis, are oten recurrent
hatcheries and seawater sites causing dark lesions requiring longer and more frequent treatments, which
in the skin, gills and internal organs, such as liver, highlights the importance of disease prevention through
kidney and musculature.15 However, the source of the good welfare and nutrition, the reduction of stress and
infection has not been identified, and treatments with the use of efective vaccines.

VET RECORD | 7
 20427670, 2018, 12, Downloaded from https://bvajournals.onlinelibrary.wiley.com/doi/10.1136/vr.104966 by BINGOL UNIVERSITY, Wiley Online Library on [12/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Vaccination are consistent in all three species. Furthermore, it is
As mortality events in cleaner fish are often associated believed that cleaner ish may act as asymptomatic
with bacterial diseases, vaccination is key to improve carriers, which poses a threat to cohabiting salmon.84
their health and welfare, improve survival and reduce Although three-day brackish water treatments have
the use of antimicrobials. Further development of proven to be efective in wrasse, it is logistically
vaccines for cleaner fish and improved vaccination impossible to carry out these treatments in commercial
strategies are required, and rapid progress has recently net pens. Commercial trials have shown that cleaner
been made in this area. ish (particularly lumpish, but also ballan wrasse)
Due to the lack of commercial (broad spectrum) can carry high numbers of amoebae compared with
vaccines available for ballan wrasse, the use of salmon despite being asymptomatic, and cleaner ish
autogenous vaccines has increased as new pathogens are oten positive for AGD using molecular methods
are regularly isolated from clinical outbreaks. long ater salmon are negative following freshwater
Autogenous vaccines currently available in Scotland bath/hydrogen peroxide treatments (C Gutiérrez,
(Ridgeway Biologicals) and Norway are aqueous-based unpublished data). As AGD appears to develop more
dip vaccines and oil-based injection vaccines, which slowly in cleaner ish than salmon, they should be
are regularly reviewed based on emergent diseases in screened using RT-PCR (not scored) for AGD before they
cleaner ish to meet the needs of the industry. Under are deployed with salmon.84
experimental conditions, for instance, polyvalent While Lepeophtheirus salmonis only infects
autogenous vaccines against atypical A salmonicida salmonids, both salmonids and cleaner ish are
using a homologous strain were found to be protective susceptible to infection by Caligus elongatus, and
for ballan wrasse with a relative per cent survival (RPS) motile stages of C elongatus can move between farmed
of 79 per cent and 91 per cent at LD50 and LD60.100 salmonids and wild ish, especially when water
Several vaccines are available for lumpish including temperatures are high.1
an injection vaccine against atypical A salmonicida VHS has caused high mortalities in both wild
(A-layer type VI) and Listonella anguillarum (syn. V wrasse90 and lumpish.92 Therefore, more research
anguillarum) serotype O1 and O2a antigens supplied on how cleaner ish can act as reservoirs of notiiable
by Pharmaq (Zoetis) and an autogenous vaccine against pathogens is required to mitigate the risks of cohabiting
A salmonicida and Vibrio salmonicida supplied by with salmon. Ballan wrasse (and corkwing wrasse, S
Vaxxinova Norway AS. In a recent trial, ish vaccinated melops) are susceptible to PMCV, and although they may
against atypical A salmonicida showed high levels not develop clinical CMS, they can pose a signiicant
of speciic antibodies, providing 73 per cent and biosecurity risk to salmon, especially if reused or moved
60 per cent RPS in monovalent and trivalent vaccines, between sites or pens.93
respectively, providing strong evidence that the Lumpish are carriers of P salmonis, and it is present
optimisation of vaccines will improve the immunity of at most sites where they are deployed,82 which may
cleaner ish to speciic diseases.101 increase infection pressure on Atlantic salmon, so it is
important that both species are treated synchronously.
Cohabitation
As both wild-caught and farmed cleaner fish are Knowledge gaps and challenges
used for the control of sea lice in salmon net pens, Cleaner fish farming is still in its infancy, and while
the culture intensification of these species may lead research is progressing rapidly with strong scientific
to the emergence of novel diseases. Farmed cleaner communities in the UK and Norway collaborating
fish are usually tested for atypical A salmonicida, together, much of the basic knowledge regarding the
Vibrio, Pasteurella (lumpfish) and AGD before they are species’ biology, their environmental and nutritional
transferred to sea pens, but this is not always the case requirements, their social and delousing behaviour and
for wild-caught wrasse, and their introduction to net their immune functions remains unknown or poorly
pens should always be risk-assessed. described. The simultaneous domestication of two new
Farmed salmon are fully vaccinated and protected marine aquaculture species is a significant challenge that
against the majority of signiicant bacterial pathogens demands sustained effort and funding over a prolonged
and viruses, including typical A salmonicida, V period of time. Research must focus on enhancing the
salmonicida and some viruses, such as IPN and robustness of the farmed stocks (better survival in the
pancreas disease.102–104 However, cleaner ish may act hatchery, reduced prevalence of malformations and a
as reservoirs/carriers for other potential pathogens, disease-free status) and increasing hatchery outputs to
for example, M viscosa, P salmonis, T maritimum or meet the urgent demands from the salmon sector and
possibly notiiable diseases, such as VHS. to protect wild stocks from overfishing. As there are
AGD afects salmon,105124 ballan wrasse85 and no selective breeding programmes for cleaner fish to
lumpish,84 and cohabitation is likely to increase the date, current research is focusing on improved larval
risk of disease outbreaks as histopathological changes and juvenile performance through better microbial

8 | VET RECORD
 20427670, 2018, 12, Downloaded from https://bvajournals.onlinelibrary.wiley.com/doi/10.1136/vr.104966 by BINGOL UNIVERSITY, Wiley Online Library on [12/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
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Competing interests None declared. (Cyclopterus lumpus L.) maintained in open net-pens with Atlantic salmon (Salmo
© British Veterinary Association (unless otherwise stated in the text of the article) salar L.). Aquaculture 2015;436:47–51.
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