Sea lice and salmon farms
Letter to Simon Coveney, Irish Minister for Agriculture, Food, and Fisheries 10 May, 2013 from
Dr Mark J. Costello, Associate Professor Institute of Marine Science, University of Auckland.
Chair of the World Register of Marine Species President of the International Association of Biological Oceanography Vice-Chair of the Global Biodiversity Information Facility Science Committee Treasurer of the Society for the Management of Electronic Biodiversity Data Marine and Freshwater Editor of the journal Biological Conservation Manager of Marine Research Information (email) NEtwork on biodiversity; archives
Papers attached to this letter by Mark Costello:
‘Ecology of sea lice parasitic on farmed and wild fish’
‘The global economic cost of sea lice to the salmonid farming industry’
‘How sea lice from salmon farms may cause wild salmoniod declines in Europe and North America and be a threat to fishes’
• 2004-present Associate Professor in Marine Ecology at the University of Auckland. • 2000-2004 Executive Director of the Huntsman Marine Science Centre, St Andrews, New Brunswick, Canada. • 1997-2000 Founding Managing Director and Chief Scientist with Ecological Consultancy Services Ltd (EcoServe), a company specialising in ecological research and consultancy in Ireland. • 1990-1997 Research and Teaching Fellow (equivalent to Lecturer and Senior Lecturer) in Environmental Sciences, Trinity College, Dublin. • 1988-1990 Research Fellow in Ecotoxicology of Napier University (Edinburgh) based at the Scottish Office Marine Laboratory (Aberdeen and Loch Ewe). • 1987 Royal Irish Academy and Royal Society postdoctoral fellowship at the Marine Biological Association, Plymouth. • 1987 National University of Ireland (Cork), PhD Zoology • 1982 National University of Ireland (Galway), BSc (Honours) Zoology
From: Mark Costello - Leigh Marine Sent: Friday, 10 May 2013 1:37 p.m. To: '[email protected]' Cc: '[email protected]' Subject: sea lice on farmed and wild fish
Dear Minister;
I have been surprised at some of the recent incorrect information in the media about whether sea lice from salmon farms can cause problems on wild fish. I have conducted research on this issue since the early 1990’s, including publishing two reviews on the subject (attached), and I was a Technical Consultant to the Aquaculture Licence Appeals Board in its early years. Several subsequent papers to my attached reviews have further supported their conclusions. I do not normally get involved in such debates but felt it important that I provide you with best scientific information. I summarise the facts below, which are supported by references to the scientific literature in the attached papers.
How sea lice from salmon farms can spread to wild fish Salmon lice emanating from farms have been linked to epizootics (mass fatal parasite infestations) on wild salmonids (salmon, trout and their relatives) in Ireland, Scotland, Norway and Canada. These epizootics are unusual in being mass infestations of the earliest life-stages of salmon lice (called the ‘chalimus’) on salmonids migrating from rivers to the sea. This means the fish were all infected at the same time as they entered the sea. They have only been reported in locations with salmon farms. When high numbers of lice occur naturally on wild fish, they usually have chalimus, immature pre-adult and adult lice. Other species of lice on salmonid farms in Chile are infesting wild fish there. These problems have not occurred in countries with low salmon farm production. Could the repeated epizootics in different years in the same places and in different places with salmon farms all be coincidences? Correlations do not prove cause; so what is the mechanism as to how lice from farms infest wild fish? Sea lice, especially the larger of the two common species called Lepeophtheirus salmonis or salmon louse, have proven difficult to control on farms, especially large farms because it is difficult to treat all fish simultaneously against the parasite, and where several farms occur in the same area due to cross-infection. The salmon louse has developed resistance to the most effective pesticides (variously called drugs, medicines, chemicals) and not all of them can be applied in all situations. The chalimus imbeds itself into the fish and grazes on the skin and mucus. Being small, a few cause little harm, but small fish have been found with tens to a hundred and more each. Once the chalimus moult into an adult stage their impact is much greater. The adults swim over the fish skin and graze it, sometimes grazing through the skin and muscle to expose the bone. All lice will irritate fish and perhaps alter their behaviour, but heavy infestations result in bleeding, may cause secondary infections, and lead to fish death. An average of five adult lice per fish generally triggers treatment on farms because such levels indicate stress to the fish and that some fish may have pathogenic levels. Each female louse can produce several batches of eggs, each containing hundreds (up to 1,000) of eggs, over her life-time. The more hosts, the more lice. If there are a million fish on the farm with 1 egg-bearing louse each, the farm may release 500 million lice larvae. So the number of fish on the farm as well as the average number of lice is key to the problem. In this example, even if there is only 1 in 10 fish with an egg bearing louse; that is potentially 50 million lice larvae. A key consequence of this is that on large farms, it is possible to keep the number of lice below what is harmful to the farm fish but they may still be producing a lot of lice larvae. The larvae (called nauplii) do not feed and swim in the plankton until they moult into the infective stage called a copepodite. The copepodite antennae are like grappling hooks and it actively searches for a host. It swims towards the surface during the day. Surface waters tend to blow towards the shore due to the day-time onshore winds. Thus the copepodites are moved towards the seashore and into estuaries so they congregate in the path of salmonids migrating to sea. If there is freshwater on the surface they will not swim into it but may get moved up the estuary in a mid-depth counter-current common in estuaries. Hydrographic models of water currents have been verified with field data on copepodite distribution. Studies in Ireland, Scotland, Norway, and Canada involving computer models and field data on infestations indicate that lice from farms may infest wild fish up to a distance of 30 km (i.e. there was no effect detected beyond 30 km). Similarly one may expect farms within 30 km of each other to be cross-infecting. Of course, not all salmon farms get problems with sea lice, and should they occur there are several ways to deal with them. The most effective method is to remove all fish from the farm and leave it fallow for some weeks. Shortening the period the salmon are on the farm will limit the build of lice. Fallowing will also break the cycles of other diseases that may occur on the farm and allow the seabed to recover from waste deposition. If there is no farm acting as a source of lice then it may be many months before re-infestation occurs from the few wild fish that may occur in the area. Like any use of the environment for farming there can be environmental impacts. It appears that sea lice are the most significant impact of salmon farms generally by virtue of their impact on wild salmonids.
I hope you find this information helpful in your decisions. I will be in Ireland next week and contactable at 087 239 339 0 if you wish to discuss further.
I have recently been contacted by Mr Tony Lowes of Friends of the Irish Environment for information about sea lice so I will send him this same information as well.
Please confirm receipt of this email.
Yours sincerely Mark Costello
><> ><> ><> ><> ><> ><> ><> ><> ><> ><> Dr Mark J. Costello, Associate Professor, Institute of Marine Science, University of Auckland.
Postal address: Leigh Marine Laboratory, PO Box 349, Warkworth 0941, New Zealand. Delivery address: 160 Goat Island Road, Leigh, New Zealand.
Direct tel. +64-9-3737599 ext 83608; Reception +64-9-422 6111. Fax +64-9-422 6113; Mobile +64-21-186 9878. Skype: markcostello Email [email protected]
Websites http://tiny.cc/vyybe www.biodiversity.auckland.ac.nz Publication citations http://scholar.google.com/citations?hl=en&user=vZue3Y4AAAAJ Other websites: Chair of the World Register of Marine Species www.marinespecies.org President of the International Association of Biological Oceanography www.iabo.org. Vice-Chair of the Global Biodiversity Information Facility Science Committee Treasurer of the Society for the Management of Electronic Biodiversity Data www.smebd.eu Marine and Freshwater Editor of the journal Biological Conservation Manager of Marine Research Information (email) NEtwork on biodiversity; archives at https://listserv.heanet.ie/marine-b.html.
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How sea lice from salmon farms may cause wild salmonid declines in Europe and North America and be a threat to fishes elsewhere
Mark J. Costello
Proc. R. Soc. B published online 8 July 2009 doi: 10.1098/rspb.2009.0771
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Proc. R. Soc. B doi:10.1098/rspb.2009.0771 Published online
Review How sea lice from salmon farms may cause wild salmonid declines in Europe and North America and be a threat to fishes elsewhere Mark J. Costello* Leigh Marine Laboratory, University of Auckland, PO Box 347, Warkworth, New Zealand Fishes farmed in sea pens may become infested by parasites from wild fishes and in turn become point sources for parasites. Sea lice, copepods of the family Caligidae, are the best-studied example of this risk. Sea lice are the most significant parasitic pathogen in salmon farming in Europe and the Americas, are estimated to cost the world industry E300 million a year and may also be pathogenic to wild fishes under natural conditions. Epizootics, characteristically dominated by juvenile (copepodite and chalimus) stages, have repeatedly occurred on juvenile wild salmonids in areas where farms have sea lice infestations, but have not been recorded elsewhere. This paper synthesizes the literature, including modelling studies, to provide an understanding of how one species, the salmon louse, Lepeophtheirus salmonis, can infest wild salmonids from farm sources. Three-dimensional hydrographic models predicted the distribution of the planktonic salmon lice larvae best when they accounted for wind-driven surface currents and larval behaviour. Caligus species can also cause problems on farms and transfer from farms to wild fishes, and this genus is cosmopolitan. Sea lice thus threaten finfish farming worldwide, but with the possible exception of L. salmonis, their host relationships and transmission adaptations are unknown. The increasing evi- dence that lice from farms can be a significant cause of mortality on nearby wild fish populations provides an additional challenge to controlling lice on the farms and also raises conservation, economic and pol- itical issues about how to balance aquaculture and fisheries resource management. Keywords: Caligus; Lepeophtheirus; trout; epizootics; aquaculture; ectoparasites
1. INTRODUCTION The best-studied example of this interaction has been Floating sea cages (or net pens) allow free movement of the epidemiology of sea lice, namely, the ectoparasitic pathogens between farmed and wild finfish. Modern copepod crustaceans Lepeophtheirus salmonis (Krøyer) and mollusc culture similarly exposes farm stock to natural several species of the genus Caligus; recently reviewed by pathogens, but is at similar densities as found in nature, Costello (2006). Their life cycle consists of non-feeding for example, in mussel and oyster beds. However, even planktonic larvae (nauplii), an infective planktonic copepo- at low farm stocking densities, sea-cage culture holds dite,1 immature ‘chalimus’ embedded on the host skin fishes for months in the same location at high host den- and mobile pre-adults and adults that move freely over sities; a situation that does not occur in nature for such the host skin. Sea lice are the most pathogenic parasite in long time periods (Bergh 2007). These conditions facili- salmon farming and may cost the industry E300 million tate disease and parasite transmission within the farm (US$480 million) a year and 6 per cent of product value (Murray & Peeler 2005). Thus, should pathogens (Costello 2009). The planktonic larvae and mobile adults from wild hosts infest a farm, their population may infest farmed fishes from natural populations and adjacent grow exponentially and release the pathogens back into farms, but their progeny are then released from the net the same environment (Murray 2008). Depending on pens into the surrounding environment where they may how the pathogen finds new hosts, the behaviour and infect wild hosts. ecology of the wild hosts and local hydrographic con- ditions, this may or may not have a significant impact (a) Epizootics on the wild fish populations. The sea lice interaction Sea lice epizootics (exceptionally heavy and fatal infesta- between aquaculture and wild fish stocks has important tions) appear to be rare in wild fish populations. However, implications for the management and viability of both it is possible that heavily infested fishes die and are not resources (Rosenberg 2008). observed, and evidence from wild fish species, including salmonids, suggests that pathogenicity may occur naturally (Costello 1993, 2006; Hvidsten et al. 2007). *[email protected] In 1989, sea lice epizootics were recorded on wild sea Electronic supplementary material is available at http://dx.doi.org/10. trout, Salmo trutta L., in Ireland for the first time, and 1098/rspb.2009.0771 or via http://rspb.royalsocietypublishing.org. it was proposed that salmon farms were the primary
Received 5 May 2009 Accepted 15 June 2009 1 This journal is # 2009 The Royal Society Downloaded from rspb.royalsocietypublishing.org on 8 July 2009
2 M. J. Costello Review. Sea lice and salmonid decline source (Tully & Whelan 1993). Similar epizootics were were due to farm lice progeny infesting wild fishes. A found on wild salmonid species in Scotland, Norway similar debate arose in British Columbia when epizootics and British Columbia, including sea trout, char Salvelinus were observed on juvenile pink and chum salmon (e.g. alpinus (L.) and pink salmon Oncorhynchus gorbuscha Brooks & Stucchi 2006; Krkosˇek et al. 2008; Diana (Walbaum). In all cases, they only occurred in regions 2009). The anti-fish farming lobby added sea lice to where Atlantic salmon was farmed in net pens (e.g. their criticisms of the industry, and government agencies Tully et al. 1999; Butler 2002; Gargan et al. 2003; prevaricated owing to insufficient knowledge. Such Krkosˇek et al. 2005, 2006b; Morton et al. 2004, 2005) debate is part of the scientific process. However, at and were characterized by heavy infestations of chalimii. some point, a synthesis is required to advise policy In Europe, epizootics were also characterized by the makers on the risk posed by sea lice from farms to wild premature return of the juvenile sea trout to freshwater fisheries. Recently, a series of papers by independent (Birkeland 1996; Gargan et al. 2003; Hatton-Ellis et al. groups of researchers from different countries have 2006). In British Columbia, juvenile pink salmon heavily provided models and data of how lice infestations can infested with sea lice have been observed to congregate occur for the salmon louse, L. salmonis. This marks a where freshwater streams mix with sea water, such as milestone in understanding the ecology of sea lice, but under waterfalls, but whether this is a response to sea perhaps more importantly, in how aquaculture may lice or not requires further research (A. Morton in impact on wild fish populations. Here, these findings Minutes of the Sea Lice Meeting of Scientists, Simon are brought together to clarify what is now known, what Fraser University, 26 March 2002 & 2008, personal further research is required (see the appendix in the elec- communication). Thus, whether lice-infested salmonids tronic supplementary material) and what are the policy exhibit freshwater return in Atlantic or Pacific Canada implications for aquaculture, and fisheries conservation. remains uncertain. A return to freshwater is beneficial to the host, because it results in reduced osmoregulatory stress and loss of sea lice (Wagner et al. 2004; Wells et al. 2. RESEARCH PROGRESS 2006, 2007; Webster et al. 2007). However, even if (a) Larval dispersal and transport epizootics and altered wild fish behaviour occur in areas The most significant progress in the understanding of sea with salmon farms, such correlation does not indicate lice in recent years has been the new data on larval disper- cause and effect unless the observations become suffi- sal, associated with oceanographic, mathematical and ciently repeated in space and time that other factors can conceptual models. Significant correlations between lice be ruled out and are supported by experimental data. abundance on farms and wild sea trout repeated over The occurrence of epizootics on both wild and farmed several years in Ireland suggested that lice may disperse fishes may have been caused by their sharing environments for up to 30 km (Tully et al. 1999; Gargan et al. 2003). that favoured the parasite, such as the location of most Field data from British Columbia and Scotland, salmon farms in wave-sheltered coastal inlets. Other supported by dispersal models, indicated that lice larvae reasons proposed as to why sea lice may not be contribut- could be transported 30 km in one area (Krkosˇek et al. ing to significant wild fish mortality have included that: 2005), concentrated in patches (Murray 2002) and their Atlantic salmon and sea trout populations had been dispersal was influenced by hydrographic conditions and declining for decades before farming began; infested wind-driven circulation (Murray & Gillibrand 2006; fishes would have died from other causes; lice may have Amundrud & Murray 2009). A review of dispersal dis- other wild hosts than farm fishes and whether the lice tances of larvae of other marine species in relation to burdens observed were pathogenic (McVicar 2004). the range of typical coastal ocean current conditions The rarity of sea lice larvae in plankton samples (except further suggested that lice larvae may disperse an average close to salmon pens), and limited knowledge of their be- of 27 km (11–45 km range) over 5–15 days, depending haviour, made it difficult to understand how lice from on current velocity (Costello 2006). farms could cause mass infestations on wild fishes many Earlier studies had found that L. salmonis had a greater kilometres distant (Pike & Wadsworth 2000). When the tolerance to low salinity than Caligus species and survived epizootics of sea lice on juvenile pink salmon later arose longer when attached to the host than free-swimming, in British Columbia, the same issues were debated in suggesting some adaptation to survival in estuarine this context with two additions. First, that infestations conditions (reviewed in Costello 1993, 2006). Thus, the of wild fishes may have been limited if the lice were reduced salinities to which migrating pink and chum washed out of inlets in low salinity currents that would (Oncorhynchus keta (Walbaum)) salmon are normally also have compromised lice development and survival. exposed to in British Columbia are unlikely to signifi- Second, there were the study-specific arguments about cantly affect survival of L. salmonis (Connors et al. how appropriate the different mathematical models and 2008a). Salmon lice abundance has been found to be choice of wild fish data were, and these have been reduced on salmon in farms in areas of low salinity in addressed in responses in the literature (Brooks 2005; Scotland (Revie et al. 2003), Norway (Heuch et al. Brooks & Stucchi 2006; Krkosˇek et al. 2006a, 2008; 2009), British Columbia (Jones & Hargreaves 2007), Brooks & Jones 2008). and for Caligus rogercresseyi in Chile (Bravo et al. In the absence of good information on sea lice ecology, 2008). However, in contrast to lice on fishes in sea the controversy about whether lice from farms were sig- cages, lice on wild and feral salmon may not be exposed nificantly impacting wild fishes grew, and scientists were to low salinities for long enough to affect their abundance unable to provide the same interpretations of available until the fishes migrate into freshwater. Experiments in data (McVicar 2004); most notably whether the corre- the laboratory and sea pens have shown that L. salmonis lations between lice abundance on farms and wild fishes copepodites swim upwards towards light and do not
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Review. Sea lice and salmonid decline M. J. Costello 3 cross into low salinity waters (Heuch 1995; Heuch et al. wind advects surface water river 1995; Bricknell et al. 2006). Plankton sampling discov- towards seashores and up estuary freshwater ered higher densities of L. salmonis copepodites in very shallow water along the seashore and in estuarine areas copepodites of Ireland and Scotland (Costelloe et al. 1995, 1998; land McKibben & Hay 2004). While the same copepodite distribution may be expected in British Columbia, it mid-water counter-current requires confirmation because the Pacific and Atlantic populations of L. salmonis are genetically distinct (Tjensvoll et al. 2006; Todd et al. 2006) and may have different evolutionary adaptations. Thus, at least in sea Europe, empirical data indicated that the infective cope- nauplii copepodites swim podites of L. salmonis concentrated in the path of up towards light migrating salmonids in estuaries. However, whether Figure 1. Diagram of how larvae of L. salmonis move into an these copepodites arose from salmon entering rivers to estuary. Nauplii may be entrained and transported in a mid- spawn, escaped farm fishes, farms or wild fishes further off- water current that runs counter to the seaward freshwater shore, was uncertain. Since then, extensive plankton current. Copepodites swim to the light and may be dispersed surveys in a Scottish sea loch supporting a wild salmon towards the seashore and up the estuary (inland) in wind- population have indicated that gravid L. salmonis on driven surface water. Solid lines indicate water flow direction. farmed salmon were the major contributor to sea lice Heavy dashed lines indicate wind-driven water movement. Dotted lines indicate movement of copepodites. larvae recovered from the plankton (Penston et al. 2008a,b; Penston & Davies 2009). A conceptual model of how larvae of L. salmonis may be transported to intercept migrating salmonid hosts (b) Identifying lice origin proposed that copepodites swim to the surface during While the presence of L. salmonis chalimii on Atlantic and daylight where the onshore wind moves the surface Pacific salmon sampled in offshore seas indicates that water towards the shore and into estuaries (Costello infestation may occur there (reviewed by Costello 2006)(figure 1). Gillibrand & Willis (2007) mathemat- 2006), the most significant infestations will occur in ically demonstrated such a model for the dispersal of coastal waters owing to the congregation of hosts, larval sea lice larvae under typical coastal environmental behaviour and hydrography. The timing of salmonid conditions (including tidal, riverine and wind-driven migrations is important in L. salmonis infestations and currents) and showed that inclusion of larval behaviour similar in both the Atlantic and Pacific Oceans. The in the model best explained field observations of copepo- juvenile salmon migrate from rivers to the sea in spring dite distribution. In addition, their hydrographic model (mainly April to May), whereas adults return to the showed how below the seaward freshwater current is an coast during the summer (mainly June to October) upstream mid-depth current that can transport larvae before entering the rivers to spawn; where their lice will towards land and into estuaries (figure 1). While some die in freshwater (Dill et al. 2009). Thus juvenile fishes model studies (e.g. Brooks & Stucchi 2006; Gillibrand & will suffer less exposure to lice transferred from returning Willis 2007) suggested that lice larvae could be washed adults the sooner they migrate away from the coast, a situ- out of inlets during high freshwater flows, other models ation called migratory allopatry between host and parasite found that gyres within sea lochs could retain larvae (Krkosˇek et al. 2007a). The source of the sea lice causing (Gillibrand & Amundrud 2007). Importantly, such the epizootics on juvenile salmonids in spring must be models may be misleading if larvae avoid entrainment in either wild salmonids that did not migrate offshore, freshwater as laboratory experiments indicate (discussed escaped or feral farm fishes, salmon farms or non-salmonid earlier). Larvae may thereby avoid salinity-delayed devel- wild hosts. Escaped farm fishes are a significant reservoir opment or mortality, and seaward transport, and be of lice in Norway in comparison with wild salmonids retained in the inner estuaries as plankton sampling (Heuch & Mo 2001), but whether they may be a reservoir suggests (Amundrud & Murray 2009). Naturally, elsewhere is not clear. variation in wind force and direction owing to weather In British Columbia, mobile L. salmonis have been conditions and landscape, and in current speed and direc- found to increase on inshore juvenile salmonids coincident tion owing to seabed topography, will further affect water with the return of adult salmon from the open ocean to movement and larval dispersal. Whether a freshwater spawn in rivers, indicating that adult sea lice transferred current is present or absent, wind-driven surface currents from returning wild salmon to farm, and to wild juvenile, are critical in larval dispersal (Amundrud & Murray salmonids (Krkosˇek et al.2007a; Saksida et al.2007a; 2009). Penston et al. (2008b) sampled plankton at Gottesfeld et al.2009). A similar phenomenon may be 0 and 5 m depth (in the absence of a freshwater surface expected in other regions with migratory salmonids. layer) and found sea lice nauplii most abundant at 5 m, Furthermore, large adult Pacific and Atlantic salmon but copepodites at the surface. Thus copepodites would returning to spawn typically have several ovigerous (egg be subjected to dispersal by wind-driven surface currents, bearing) lice, which will release their larvae inshore. If and nauplii most abundant near their sources (e.g. these lice find new hosts before the host enters freshwater, farms), as Costelloe et al. (1995) found in Ireland and they may produce more strings of eggs as lice on farm Penston et al.(2008a,b) in Scotland. Comparable fishes do. Beamish et al.(2007)found that although plankton sampling has not been reported in Canada or most fishes migrate away from the coast, some individuals Norway, nor for any Caligus species. of adult and juvenile Pacific salmon were present in coastal
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4 M. J. Costello Review. Sea lice and salmonid decline waters of British Columbia throughout the year and 2009). It recognizes a host’s movement by mechanosen- provided a continuous reservoir of sea lice. Similarly, in sors from approximately 26 mm distance (Heuch et al. European seas, some wild salmonids, such as sea trout 2006), but may also be attracted by water-borne host S. trutta, and farm escapes, may be present in coastal odours, as well as contact chemosensors once attached waters most of the year. However, over 90 per cent of to the host (Mordue Luntz et al. 2006; Fields et al. Atlantic salmon in Irish, Scottish, Norwegian and Gulf 2007; Pino-Marambio et al. 2007; Mordue & Birkett of Maine (New Brunswick, Atlantic Canada, and Maine, 2009). Both copepodite and adult lice can discriminate USA) coastal waters are in farms (e.g. Tully & Whelan their preferred host species using both odour and taste, 1993; Heuch & Mo 2001; Butler 2002; McKenzie et al. and pre-adult female lice attract males using pheromones 2004). Despite the greater abundance of wild Pacific com- (Mordue & Birkett 2009). pared with wild Atlantic salmon, most Pacific salmon are Mobile (pre-adult and adult) sea lice can transfer offshore until the summer (reviewed by Krkosˇek in between hosts, and Caligus mobiles are found in the press), and Orr (2007) predicted significant lice pro- plankton (Hewitt 1971; Costello 2006;A.Morton2008, duction (billions of larvae) from farms in British Columbia unpublished data). The rapid arrival and loss of C. elongatus from 2003 to 2004. Atlantic salmon are typically grown in from fish farms suggest that transmission by mobiles is sea pens for about 18 months and so can provide a signifi- significant. Mobile L. salmonis can transfer from returning cant reservoir of sea lice all year around. Pacific salmon to migrating juvenile pink salmon (discussed While Caligus species seem to have wide host prefer- earlier). Another method of transmission may be for lice to ences, L. salmonis is largely restricted to, and only matures transfer to a predator of their host. Connors et al.(2008b) on, salmonids. Even wild non-salmonid fishes congregated found 70 per cent of L. salmonis (mostly males) transferred around salmon pens in Scotland (Bruno & Stone 1990) from their host when it was predated. In this instance, the and Ireland (M. J. Costello 1994, unpublished data), and host was also a salmonid. Were it a less suitable host, the wrasse held within salmon pens (Costello et al.1996), do lice may transfer again when an opportunity arose. Thus, not host this species. In British Columbia, field surveys transmission of mobile stages may be important for lice found that not only were juvenile pink and chum salmon but is largely unstudied. It would enable redistribution of infested, but 84 per cent of sticklebacks Gasterosteus lice among hosts so as to prevent pathology, leading to aculeatus L. also were, of which 97 per cent were copepo- host mortality and loss of lice habitat. By increasing the dite and chalimus stages (Jones et al.2006a). However, number of hosts infested, it would further spread the lice laboratory studies found a loss of lice on all three hosts population. Hosts may be attracted to what appears to be over time, and no mature L. salmonis occurred on stickle- a crustacean prey item in the plankton, but upon approach, backs (Jones et al.2006b). Neither the source nor fate of the lice may dodge predation and attach to the host, as these lice was known, but some may re-infest other fishes. aquarium observations indicate may occur (Connors et al. Thus sticklebacks may act as a temporary reservoir for 2008b; M. J. Costello 1993, personal observation). This L. salmonis, albeit not as significant a reservoir as hosts of transmission of adult life stages may be more important ovigerous lice. Because the epizootics on juvenile for Caligus than for Lepeophtheirus species, as only the salmonids consist of the same early life-stages as found former are commonly found in the plankton. The success on sticklebacks, it is likely that both are receiving lice of mobile louse transmission may vary with light conditions from the same sources rather than contributing to each as found for ectoparasitic isopod praniza larvae (Smit & other’s infestations. Davies 2004). Experiments on the behavioural interactions Efforts to find indicators of whether juvenile lice on wild between mobile lice and their hosts are required to fishes have come from farmed fishes have met little success. understand the significance of this route of infestation. Although it is possible to distinguish lice from farmed and wild fishes using stable isotopes, elemental signatures and colourants derived from feeding on farmed fishes, these (d) Host impacts indicators do not identify farm lice progeny that may It had been suggested that lice may preferentially infest infect wild fishes (Todd 2006). Genetic analyses indicate and cause mortality to weaker fishes that would have that L. salmonis is one well-mixed population across the died from other causes (McVicar 2004). However, Todd North Atlantic, but that there has been some genetic drift et al. (2006) found that wild Atlantic salmon in poor from the North Pacific population; thus genetics are unlikely condition were not more likely to have high lice burdens. to distinguish farm and wild host populations (Costello At low density (less than three lice per fish or less than 2006; Todd 2006). While Caligus elongatus von Nordmann 0.65 lice g21 fish), lice had no effect on the condition of has two genotypes in the North Atlantic, whether they juvenile pink salmon (Butterworth et al. 2008). Even have diverged based on seasonal reproductive cycles, host high densities of chalimus on sticklebacks in British selection or other environmental factors remains to be Columbia did not correlate with fish condition (Jones determined (Øines & Heuch 2007). However, indirect sup- et al. 2006a). Comparable studies have not been con- port from spatial transmission models indicates that farms ducted for farm fishes. Similarly, helminth parasites do can be significant sources of lice on wild fishes (Krkosˇek not appear to normally affect host condition and mor- et al. 2005, 2006b;Frazer2008, 2009). tality (reviewed by Thomas 2002). In an evolutionary context, this benefits the survival of both the parasite and its (host) habitat. Higher parasite burdens on fishes (c) Host capture in better condition may reflect the occurrence of more In the vicinity of a host, the L. salmonis copepodite parasites in locations where the fishes find more food. increases swimming speed and attaches faster to slower Lice can cause reduced swimming and cardiac moving hosts (Genna et al. 2005; Mordue & Birkett performance in Atlantic salmon (Wagner et al. 2004).
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Although lice-infested fishes show increased leaping Clupea harengus L. and haddock Melanogrammus behaviour, presumably to dislodge lice (Stone et al. aeglinfinus (L.) (reviewed by Costello 1993), and sub- 2002), which may attract predators, it would seem disad- populations may have host preferences (Øines et al. vantageous for the host to be predated because the lice 2006). Infestation of bluefin tuna, Thunnus maccoyii may not easily find an alternative host (but see above). Castelnau, in farms in South Australia by mobile Caligus At present, whether fishes suffer more or less predation chiastos Lin & Ho (2003) and Caligus amblygenitalis owing to lice infestation is unknown. However, a compari- Tripathi (1961) resulted in host blindness and reduced son of lice abundance between wild fishes and epizootics weight (Hayward et al. 2008, 2009). The absence of suggests that lice may sometimes be sufficiently abundant chalimus stages indicated direct transfer of mobile lice to cause host mortality under natural conditions (Costello from wild hosts. A candidate aquaculture fish species in 2006). Australia, mulloway Argyrosomus japonicas (Temminck & Recent reviews have stated that greater than 0.5 to Schegel), can be infested by another Caligus species tenta- 0.75 mobile L. salmonis per gram host weight, or more tively identified as C. elongatus (Hayward et al. 2007). than 5 to 10 per fish (greater than 0.1 lice g21 fish) can While Caligus spinosus Yamaguti infests farmed yellowtail be pathogenic to Atlantic salmon, Salmo salar (Costello amberjacks Seriola quinqueradiata Temminck & Schlegel 2006; Wagner et al. 2007). Todd et al. (2006) found in Japan, the larger C. lalandei Barnard has appeared in that 0.2 to 0.7 L. salmonis per gram were pathogenic to the region on wild yellowtail and may cause more severe the sea trout S. trutta. Although chalimii are not known infestations on farms (Ho et al. 2001). A variety of wild to be pathogenic, they can become so when they mature and farmed marine finfish species from Australia to into mobile stages if sufficiently abundant. Survival southeast Asia have had pathogenic infestations of Caligus models for juvenile pink salmon indicated significantly epidemicus Hewitt (Ho 2000; Ho et al. 2004). Although greater population mortality if L. salmonis abundance only 1–3 mm in size, C. epidemicus may hold the record was greater than or equal to 0.75 or 2.0 mobile lice per for lice abundance on a single host; over 5000 were fish, depending on whether predators selected fish that taken from a single host surgeonfish in captivity (Ho were lice infested or not, respectively (Krkosˇek in et al. 2004). press). These pink salmon were less than 1 g in weight Young-of-the-year herring, Clupea pallasi Valenciennes so these levels are similar to levels pathogenic to the have been infected by Caligus clemensi (Parker & Salmo species. However, pathogenicity varies with host Margolis) in areas of British Columbia with high numbers size, species and other health conditions (Costello 2006; of fish farms (Morton et al. 2008). In Chile, the abun- Jones et al. 2007; Wagner et al. 2007; Bravo et al. 2008), dance of C. rogercresseyi (Boxshall & Bravo) on wild and how fish sensitivity changes with size and age needs hosts decreased after farm fallowing, indicating transfer to be better quantified (Krkosˇek in press). of lice from farm to wild hosts (C. Levicoy & Chalimus abundance during epizootics is typically G. Asencio 2009, personal communication). However, greater than 10 per fish (sometimes over 60) on sea with the possible exception of a heavy infestation of C. roger- trout and Arctic charr (Bjorn et al. 2001; Gargan et al. cresseyi on feral trout S. trutta in southern Argentina (near 2003; Heuch et al. 2005) and over three per pink and Chile) (Bravo et al.2006), sea lice epizootics have not chum salmon, which are a much smaller fish (Morton been reported on wild fishes in South America. et al. 2004). Such levels will at least irritate and stress While farm data show replacement of Caligus species the host and, when they moult to mobile stages, will be by L. salmonis on farms (Revie et al. 2002; Saksida et al. fatal (Bjorn & Finstad 1997; Tully & Nolan 2002). 2007b), there can also be positive correlations in both However, experimental studies find lice tend to be lost species abundance on farmed salmon (Todd et al. from hosts over time. Almost all pre-adult lice were 2006). Such contrasting correlations may be due to lost from wild-captured Pacific salmon hosts in laboratory density-dependent competition between the species, and sea-cage experiments (Krkosˇek et al. in press). whereby populations of both species may increase until Whether these lice die and fall off, are dislodged and the larger L. salmonis begins to displace C. elongatus. move onto a different host, are eaten by the fish or are There are little-to-no benefits of fallowing and parasiti- lost due to the experimental conditions is not clear. cides in controlling C. elongatus on farms, perhaps Data on the mortality of sea lice on wild and farmed because adult Caligus transfer between wild and farmed fishes are required for predictions about future host hosts more readily than L. salmonis (Treasurer & Grant impacts. Such estimates may be possible by monitoring 1994; Revie et al. 2002). Thus, some Caligus species lice population dynamics on farms. are already causing problems to farm and wild fish populations, and more threaten to do so. Studies on the (e) Caligus species behaviour of Caligus species’ larvae and adults are How Caligus species maximize their chance of finding required to understand how these sea lice find their a suitable host is uncertain, but appears to involve hosts (appendix in the electronic supplementary material) adults dispersing in the plankton, and moving and manage the risks of transmission between farm and between a wider range of host species than Lepeophtheirus wild fish stocks. species (Ho 2004; Costello 2006). Where L. salmonis is absent, Caligus species can be a problem on farms and (f ) Geographical extent of the problem on wild fishes and can be a more difficult parasite to The L. salmonis epizootics would have been afflicting control. juvenile salmonids in Ireland, Scotland, Norway and Species of Caligus have been pathogenic to salmonids British Columbia for some time before being observed. on farms in Europe and Chile, and observations suggest Similar epizootics may also have occurred in the Gulf of that C. elongatus can be pathogenic to at least wild herring Maine, but not have been noticed. Other pathogenic
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6 M. J. Costello Review. Sea lice and salmonid decline infestations of L. salmonis on wild salmonids, and Caligus coincident with salmon farming in both North America on other fish species, were adult populations (Hewitt and Europe (Ford & Myers 2008). However, these are 1971; reviewed by Costello 1993). Indeed, were it not general patterns. Not all salmon farms have sea lice for the premature return of heavily infested sea trout to problems, and local hydrographic conditions vary and freshwater where they were easily observed, the phenom- will influence larval dispersal. Despite improved knowl- enon may not have been discovered in Ireland. The edge about how to control sea lice on farms, including countries that produce most farmed salmonids have a pro- fallowing and a wider range of parasiticides, sea lice blem with sea lice on farms whereas the minor producers epizootics persist. In Ireland, where the impact on wild do not (see the appendix, electronic supplementary salmonids was first discovered, government monitoring material), suggesting a relationship between the number of farms found that L. salmonis abundance had increased of farms and/or farmed fishes, and the development of since 2001 after an earlier decline (O’Donohoe et al. sea lice infestations on farms. Persistent infestations on 2007), and the problem continues to be raised in the par- farms increase the risk of lice transferring to wild fishes. liament and the press (e.g. Viney 2008). Some salmon Krkosˇek et al. (2007b) estimated the mortality of pink farms will not be a source of sea lice for wild fishes, and salmon owing to L. salmonis in areas with salmon farms epizootics may not always occur in areas with salmon to be 80 per cent, levels that could extirpate populations farms. However, if one of a group of neighbouring in four generations (eight years). Two of their co-authors farms is infested, then both the farms who have lice conducted a global analysis and found a significant under control and the wild fish populations are at risk decrease in wild salmon abundance in areas with salmon of infestation. To coordinate sea lice control, industry, farming compared with areas with no farms since the late wild fishery and regulatory agencies have increasingly 1980s (Ford & Myers 2008). They compared all regions become involved in sea lice control on farms to minimize of the world where both wild and farmed salmonids risks to wild fishes. co-occurred, and thus controlled for environmental con- ditions in the freshwater and marine phases, and for fishery impacts. While salmon farming may have several impacts 4. OUTLOOK on wild stocks, including escaped farmed fishes interfering The globalization of the salmon-farming industry may in wild fish spawning and genetic dilution, the most likely help expedite the development and implementation of cause of the global decline in wild salmonids in areas with measures to improve fish health and reduce sea lice trans- farms was sea lice transmission from farms. Frazer (2009) fer to wild fishes. However, moving farm sites to reduce argues that the ‘wild fish decline in proportion to the ratio the risk of sea lice transmission and to improve coordi- of lice abundance on farm ...to ...wild fish’, largely nated fallowing requires cooperation of farm owners because each female louse produces thousands of eggs in and staff, local communities (who may object to new her lifetime so less than 0.1 per cent need to survive to farm locations) and government authorities. In some maintain the lice population. Should this be the regions, reductions in farm density would reduce overall situation, sea lice-infested farms would lead to the extirpa- farm production and may have financial consequences tion of the local wild fish population, unless the total for the companies involved and local economy. However, number of lice is less on the farm than on the wild fish this may result in a more sustainable salmon-farming population. industry and help protect wild populations. Salmon farm- ing is an important agribusiness and employer in many countries and remote coastal regions of Europe and the 3. CONCLUSIONS Americas. Fisheries for wild Atlantic salmon and sea The evidence that salmon farms are the most significant trout were once a significant economic resource, and source of the epizootics of sea lice on juvenile wild salmo- the health of Pacific salmon stocks is also of concern. nids in Europe and North America is now convincing Sea lice thus raise important social, economic and politi- (Heuch et al. 2005; Costello 2006; Krkosˇek et al. 2006b, cal issues, as well as priorities for nature conservation and 2007a,b, in press; Todd 2006). Farms may contain fish health. In addition, they provide a case study of millions of fishes almost year round in coastal waters problems that can arise in aquaculture that could be and, unless lice control is effective, may provide a con- repeated elsewhere. tinuous source of sea lice, although the amount of infesta- I thank Sandra Bravo, John Burka, Kai (Ju-Shey) Ho, Martin tion pressure will vary over time owing to seasonal and Krkosˇek, Cristobel Levicoy, Alexandra Morton, Sandy farm management practices (e.g. fallowing). If escaped Murray, Michael Penston, Jim Treasurer and anonymous farm fishes remain in coastal waters, they will be an reviewers for very helpful information and/or suggestions additional reservoir of lice. Experimental and field data on earlier versions of this paper. in conjunction with mathematical models provide an explanation of how the larvae of the most common and pathogenic species, L. salmonis, disperse and congregate to infest wild salmonids in coastal waters. The correlation ENDNOTE of epizootics on wild fishes in areas with fish farms, com- 1The term copepodite or copepodid refers to the infective plankton pared with (control) areas without farms, has been stage of Caligidae (Copepoda Crustacea). A search on Google Scholar found that the former term is most used in the scientific litera- repeated over years and in different countries (see the ture (6260 versus 3710 responses on 15 December 2008), although appendix, electronic supplementary material). Analyses the latter tends to be more used in the sea lice literature (57 versus that controlled for the effects of environmental conditions 361 results when term was combined with ‘sea lice’). There seems and fisheries found that salmon population declines were to be no benefit to have two terms for such similar life stages.
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McKenzie, E., Gettinby, G., McCart, K. & Revie, C. W. Orr, C. 2007 Estimated sea louse egg production from 2004 Time-series models of sea lice Caligus elongatus Marine Harvest Canada farmed Atlantic salmon in the (Nordmann) abundance on Atlantic salmon Salmo salar Broughton Archipelago, British Columbia, 2003–2004. L. in Loch Sunart, Scotland. Aquacult. Res. 35, 764– North American. J. Fish. Manag. 27, 187–197. (doi:10. 772. (doi:10.1111/j.1365-2109.2004.01099.x) 1577/M06-043.1) McKibben, M. A. & Hay, D. W. 2004 Distributions of Penston, M. J. & Davies, I. M. 2009 An assessment of planktonic sea lice larvae Lepeophtheirus salmonis in the salmon farms and wild salmonids as sources of inter-tidal zone in Loch Torridon, Western Scotland in Lepeophtheirus salmonis (Krøyer) copepodids in the water relation to salmon farm production cycles. Aquacult. column in Loch Torridon, Scotland. J. Fish Dis. 32, Res. 35, 742–750. (doi:10.1111/j.1365-2109.2004. 75–88. 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10 M. J. Costello Review. Sea lice and salmonid decline
louse Lepeophtheirus salmonis. Dis. Aquat. Organ. 68, 251– Lepeophtheirus salmonis (Krøyer) in relation to sources of 259. (doi:10.3354/dao068251) infection in Ireland. Parasitology 119, 41–51. (doi:10. Todd, C. D. 2006 The copepod parasite (Lepeophtheirus sal- 1017/S003118209900445X) monis (Krøyer), Caligus elongatus Nordman) interactions Viney, M. 2008 From small sea-lice do great problems grow. between wild and farmed Atlantic salmon (Salmo salar The Irish Times, Saturday 24 January 2008. L.) and wild sea trout (Salmo trutta L.): a mini review. Wagner, G. N., McKinley, R. S., Bjørn, P. A. & Finstad, B. J. Plankt. Res. 29(Suppl. 1), 161–171. 2004 Short-term freshwater exposure benefits sea lice- Todd, C. D., Whyte, B. D. M., MacLean, J. C. & Walker, infected Atlantic salmon. J. Fish Biol. 64, 1593–1604. A. M. 2006 Ectoparasitic sea lice (Lepeophtheirus salmonis (doi:10.1111/j.0022-1112.2004.00414.x) and Caligus elongatus) infestations of wild, adult, and one Wagner, G. N., Fast, M. D. & Johnson, S. C. 2007 sea-winter Atlantic salmon Salmo salar returning to Physiology and immunology of Lepeophtheirus salmonis Scotland. Mar. Ecol. Prog. Ser. 328, 183–193. (doi:10. infections of salmonids. Trends Parasitol. 24, 176–183. 3354/meps328183) (doi:10.1016/j.pt.2007.12.010) Treasurer, J. & Grant, A. 1994 ‘Second’ louse species must Webster, S. J., Dill, L. M. & Butterworth, K. 2007 The effect not be ignored. Fish Farmer 17, 46–47. of sea lice infestation on the salinity preference and ener- Tully, O. & Nolan, D. T. 2002 A review of population getic expenditure of juvenile pink salmon (Oncorhynchus biology and host–parasite interactions of the sea louse gorbuscha). Can. J. Fish. Aquat. Sci. 64, 672–680. Lepeophtheirus salmonis (Copepoda: Caligidae). Parasitology (doi:10.1139/F07-043) 124, 165–182. (doi:10.1017/S0031182002001889) Wells, A. et al. 2006 Physiological effects of simultaneous, Tully, O. & Whelan, K. F. 1993 Production of nauplii of abrupt seawater entry and sea lice (Lepeophtheirus salmo- Lepeophtheirus salmonis (Krøyer) (Copepoda: Caligidae) nis) infestation of wild, sea-run brown trout (Salmo from farmed and wild salmon and its relation to the infes- trutta) smolts. Can. J. Fish. Aquat. Sci. 63, 2809–2821. tation of wild sea trout (Salmo trutta L.) off the west coast (doi:10.1139/F06-160) of Ireland. Fish. Res. 17, 187–200. (doi:10.1016/0165- Wells, A. et al. 2007 Physiological consequences of 7836(93)90018-3) ‘premature freshwater return’ for wild sea-run brown Tully, O., Gargan, P., Poole, W. R. & Whelan, K. F. 1999 trout (Salmo trutta) postsmolts infested with sea lice Spatial and temporal variation in the infestation of sea (Lepeophtheirus salmonis). Can. J. Fish. Aquat. Sci. 64, trout (Salmo trutta L.) by the caligid copepod 1360–1369. (doi:10.1139/F07-107)
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Ecology of sea lice parasitic on farmed and wild fish
Mark J. Costello
Leigh Marine Laboratory, University of Auckland, PO Box 349, Warkworth, New Zealand
Abstract Glossary Sea lice, especially Lepeophtheirus salmonis and Caligus spp., have the greatest economic impact of Chalimus (plural chalimi): the four stages of immature lice fixed to the host by a frontal filament around which they feed on host mucus and skin. any parasite in salmonid fish farming and are also a Copepodid: post-naupliar larvae. In the case of sea lice the term refers only to threat to wild salmonids. Here, I review how the biology the free-living, non-feeding, planktonic larva that must find a host to survive, as and ecology of various louse and host species influence the next immature life-stage is called the chalimus stage. Degree days: in aquaculture, the sum of temperature degrees experienced daily their pathogenicity and epidemiology. Recent discov- (e.g. 40 days at 10 8C=4008d). It is a useful index of the temperature required for eries of new species and genotypes emphasize the need the growth and development of ectotherms within their range of tolerance. Diel: over a 24-hour period of night and day. for more basic research on louse taxonomy and host Epizootics: epidemics in non-human species. preferences. Louse development rates are strongly Fallowing: the process of leaving cages on a farm site empty of fish so as to dependent on temperature, and increasing mean sea interrupt parasite and disease cycles and/or to enable the seabed to recover from waste sedimentation. temperatures are likely to increase infestation pressure Frontal filament: an organ attaching chalimi and moulting mobiles of on farms and wild fish, as well as affecting the geogra- Lepeophtheirus salmonis to the host. phical distribution of hosts and parasites. Despite pro- Mobile lice: pre-adult and adult stages that move freely over the host fish. Commonly referred to as mobiles. gress in finding L. salmonis larvae in the plankton and in Nauplius (plural nauplii): two life-stages of free-living non-feeding planktonic modelling louse production in several countries, more larvae that hatch from the egg and moult to become copepodids. data on larval behaviour and distribution are required to Ovigerous female: a female louse carrying two conspicuous uniseriate egg strings containing a total of 100–1000 eggs. develop dispersal and transmission models for both Parasiticide: a chemical or chemotherapeutants used to kill parasites. Can be L. salmonis and Caligus spp. This knowledge could be called a medicine, pesticide, or drug in different countries. used to take measures to reduce the risks of lice affecting Pre-adult: immature mobile louse. There are two pre-adult stages in Lepeophtheirus species and there is some debate as to whether they occur farmed and wild fish. in Caligus spp. Pycnocline: a zone of rapid change in density in a water body, typically Introduction attributable to temperature and/or salinity. Sea trout: sea-running individual of the brown trout Salmo trutta L. Sea lice (Copepoda, Caligidae) have been the most wide- Smolt: juvenile salmonid fish physiologically adapted for living in seawater. The spread pathogenic marine parasite in the 30 year-old term is applied to fish immediately prior to their first migration from freshwater Atlantic salmon (Salmo salar L.) farming industry, and to the sea, and can be applied to farm fish within their first year in seawater. Uniseriate: in a single row. in the past 15 years pathogenic infestations on other cultured fish and wild salmonids have escalated [1–3]. All but one species of sea lice parasitize bony marine fish (Actinopterygii), and 54% of copepod infestations of farmed fish are caligids [4]. Their impact ranges from mild skin damage to stress induced mortality of individual fish (Figure 1, Box 1), and includes epizootics (see Glossary) in wild fish populations in Europe and British Columbia. Research has concentrated on Lepeophtheirus salmonis (Krøyer, 1837) because it has the greatest impact on Atlantic salmon farms (Box 2). However, this research has wider implications because other crustacean ectopara- sites, including other caligids and isopods, are pathogenic to salmonids and other cultured finfish [1,4–6]. Four spe- cies of Caligus occur on farms in British Columbia, Chile, Europe and Japan (BoxAuthor's 2). personal copy Eggs carried by the female louse hatch into non-feeding planktonic larvae that infect a new host (Box 3). How these larvae disperse and find a new host has been one of the most challenging issues, because of its relevance to Figure 1. A typical heavy infestation of an Atlantic salmon by the sea louse Corresponding author: Costello, M.J. ([email protected]). Lepeophtheirus salmonis, showing removal of skin over the head, and female lice Available online 21 August 2006. bearing paired egg-strings on the back. Reproduced with permission from Alan Pike. www.sciencedirect.com 1471-4922/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.pt.2006.08.006 476 Review TRENDS in Parasitology Vol.22 No.10
Box 1. Sea louse pathogenicity Box 2. Sea lice in salmon farms
Sea lice use rasping mouthparts to graze the host and remove Lepeophtheirus salmonis parasitizes Salmonidae in the northern mucus, skin and underlying tissues [1] (Figure 1, main text). They hemisphere oceans: it has been recorded on 12 species in the can occur anywhere on the body but often congregate on the head genera Salmo (North Atlantic salmon and trout), Salvelinus (trout in farmed and wild fish. They grip the host with their second pair of and charr) and Oncorhynchus (Pacific salmon) [2], and two species antennae and maxillipeds. Mobile sea lice are designed so that of cyprinids in marine waters in and near Japan [9]. In Chile, Caligus water flow presses them to the host surface over which they swim rogercresseyi Boxshall and Bravo, 2000 is the dominant species on by jet propulsion. Some salmon leaping behaviour appears to be a farmed salmonids. In Japan, L. salmonis is present on farmed response to irritation by sea lice [64] and an attempt to dislodge salmonids, but it is C. orientalis Gussev, 1951 that is the more them [1]; this can attract predators, distract the fish and has energy pathogenic [9]. Caligus elongatus Nordmann, 1832 is common on costs. Impacts on the host skin include epithelium loss, bleeding, farmed salmonids in the northern hemisphere and is sometimes increased mucus discharge, altered mucus biochemistry, tissue pathogenic, and like C. orientalis (in Japan), C. clemensi Parker and necrosis and consequent loss of physical and microbial protective Margolis, 1964 (in British Columbia) and C. rogercresseyi and function [4,7]. In heavy infestations, chalimi can attach in such C. teres Wilson, 1905 (in Chile), it is not host-specific [8,72]. numbers that they can be lost from the fins as a result of skin Although L. salmonis is the most pathogenic species on Atlantic erosion. The attachment of chalimi to the gills appears to be an farms, probably because of its larger body size, it is also more artefact of laboratory conditions [65] and would explain their prevalent and persistent on farmed fish than C. elongatus. absence on the gills of wild fish [7]. However, it might also be due Salmonids are probably secondary hosts to the other Caligus to loss of copepodids from the gills following initial settlement [63]. species recorded on farmed fish, as most are known to occur on Host fish have reduced appetite, growth and food-conversion one or more wild non-salmonid hosts [8]. Nevertheless, these lice efficiency, and the stress and wounds expose fish to secondary can be pathogenic to their secondary host, and it is crucial that infections [1], to which they are more susceptible [66]. Changes to the parasites are correctly identified to understand their origins. One the host blood include anaemia, reduced lymphocytes, protein, ion species, C. rogercresseyi, was only recently described from farmed imbalance and elevated cortisol [4,7,8]. These changes indicate a salmon in Chile, where it had been mistakenly identified as stressed and weakened host, with reduced osmoregulatory and C. flexispina. Genetic analysis indicates that the apparently respiratory ability and impaired immunocompetence. In Europe, widespread C. elongatus consists of at least two genetically distinct heavily infested sea trout return to fresh water prematurely [67], populations in the North Atlantic, both occurring on the same and a suggesting that this could reduce osmoregulatory stress and/or help variety of hosts [41,72], and that North Atlantic and Pacific remove lice. Laboratory studies found swimming performance of populations of L. salmonis are distinct [35]. This demonstrates the louse-infested fish improved when transferred from sea to fresh need for continued taxonomic research on caligids and their hosts water [68]. Host blood is not an important part of the diet of sea lice, and for new identification guides. Louse species have varying as suggested by some authors, and female lice do not ingest more environmental tolerances, behaviour as adults and larvae and than males as might be the case for blood-feeding parasites [69]. growth and survival on different hosts, yet species identity has not However, physiologically significant host blood loss can occur with been well determined in studies aimed to determine whether sea high levels of louse infestation [70]. The risk that sea lice transmit lice spread from farms to wild fish [29,43]. Differences between bacterial and viral pathogens is a concern [71]. Although the risk is different host and parasite species, as well as different develop- low for L. salmonis [2,7], it is higher for Caligus species because mental stages of the host and parasite, must be clarified to prevent they occur on more host species and adults of at least C. elongatus confusion in modelling epidemiological impacts of sea lice and occur in the plankton [1]. developing integrated pest management strategies. transfer within and between fish farms and also from mature adult for L. salmonis and C. elongatus on Atlantic farms to wild fish populations. Here, I focus on the patterns salmon is 40 days at 10 8C (i.e. 400 degree days) for males of sea louse infestation and the aspects of their biology that and 10 days longer for females [1,2,10]. Generation times influence transmission, because these issues have received can be shorter for C. rogercresseyi [11], and if derived from least attention in previous reviews [2,4,7,8]. Space limita- monitoring field populations, generation times can appear tions require that references given are those published longer because cohorts are not as synchronized as in the since previous reviews on aspects of this subject laboratory [11]. In addition, development rates can vary on [1,2,4,5,7–9]. It should be noted that many observations different hosts [7]. Typically for crustaceans, sea lice live in the literature have not been replicated across localities, longer and grow larger at colder temperatures, and larger populations or species, and future studies are needed to females produce more eggs [2]. Consequently, over- test the generalizations drawn from previous studies. wintering females are larger and release more eggs in the spring than summer brooders. Because spring eggs Infestation patterns are also larger, spring larvae have greater food reserves Although the abundance of sea lice depends on their intrin- and thus they might spend longer in the plankton search- sic fecundity and rates of growth and development, it could ing for a suitable host. Laboratory studies could determine also depend on density-dependant competition within and larval viability in relation to parent body size and between species, and on host responses to infestation. Key larval size. Although summer generations of females are factors affecting these characteristics and interactions smaller and have fewer eggs per brood because of the include sea temperature,Author's and host abundance and distribu- personalshorter generation time copy at warmer temperatures, tion. The concentration of hosts on salmon farms has the summer populations can increase exponentially. The increased lice abundance locally, with consequences for lice different temperature regimes in salmon farming areas infestations on farmed and wild hosts. (1–14 8C in Atlantic Canada, 6–18 8C in Ireland and 1–20 8C in some Norwegian fjords) are thus likely to result Louse population dynamics in different sea louse population dynamics. However, Sea louse growth is strongly dependent on temperature. In further research on different sea louse species and popula- the laboratory, the generation time from egg extrusion to tions is required to explain variation in their development www.sciencedirect.com Review TRENDS in Parasitology Vol.22 No.10 477
Box 3. Sea louse life-cycles Box 4. Sea louse control on salmonid farms
Sea louse eggs are carried in a pair of uniseriate strings of 100 to The following guidelines give the best practice for sea louse control 1000 eggs extruded from the abdomen of the female [1] (Figure I). on salmonid farms [76]: The number of eggs per sea louse varies with time of year, louse To break the population cycle of sea lice, farms should have a size, louse age, host species and population and is affected on farms fallow period during which no farmed fish are present in an area by the effects of parasiticides [1]. The use of 500 eggs per sea louse for 4–6 weeks. This is facilitated by having only one year class of on farmed salmon and 1000 on wild fish for modelling louse fish per site. populations [25] would thus have been conservative in estimating Cleaner-fish should be stocked into fish cages where they are production of sea lice on farms. Further quantitative data on the available. relationship of egg production to the above variables is important In-feed parasiticides should be given to smolts in freshwater tanks for assessing infestation risks [10,73]. before transfer to sea cages and louse abundance should then be The eggs hatch in sequence from the distal end and the female monitored to guide future treatment. can produce six to eleven broods [2]. Two nauplius stages of larvae Sick (moribund) fish should be removed from sea cages and net are non-feeding and planktonic for 5–15 days (temperature-depen- fouling should be minimized to maximize water flow. dent) and moult into infective free-living copepodids that attach to a If present, lice should be treated during the winter to remove egg- host by their antennae [1]. Eggs manually removed from the female bearing females before the spring. hatch in the laboratory and can be easily reared to copepodids. Where parasiticides are used regularly in an area, louse sensitivity Evidence suggests that copepodids (i) respond visually to host (resistance) to them should be monitored. shadows and flashes from host scales, (ii) use mechanoreceptors on The health status of fish stocked into a farm should be made their antennae to respond to vibrations such as those a host creates known to neighbouring farms. and (iii) use chemoreceptors to determine host suitability (and later Prevention of escaped salmon will reduce the risks of transfer to mate detection) [2,11,74]. Recent research also indicates that other farms and wild fish. copepodids and mobile lice could use water-borne chemical cues The potential of transfer of sea lice (and other pathogens) should (semiochemicals) to recognize hosts [75]. be considered in the selection of farm sites. The copepodid moults into a chalimus that is attached to the host Cleaner-fish were the first successful use of biological control in by a special frontal filament [2]. There are four successive sessile finfish culture; they include five species of wrasse (Labridae) in chalimus stages that feed on the host skin around their point of Europe [1,77]. Wrasse remove larger lice first, thus eliminating egg- attachment. In Lepeophtheirus, but not necessarily in Caligus bearing females and do so without stressing the salmon, with species [5], there are two immature pre-adult stages that move consequent benefits in growth and food-conversion efficiency. If freely over the host skin to feed. These mobile stages attach to the wrasse escape or insufficient numbers are available, a parasiticide host with a chalimus-like filament when moulting [2]. Although treatment can be undertaken, even with wrasse in the cage. This Kabata suggested in 1972 (reviewed in [5]) that all Caligidae have practice is well-established in Norway, including the use of novel ten life-stages (two nauplius, copepodid, four chalimus, two pre- fisheries and traps and special good husbandry practices [78–80]. adult, adult), and that the apparent absence of one or two pre-adult Parasiticides against sea lice can be applied as an in-situ stages in descriptions of some Caligus species was an oversight by ‘bath’ by enclosing the salmon cage in a plastic covering, or researchers (including himself), a recent review considers Caligus they can be mixed with the food pellets as ‘in-feed’ treatments [1]. species to have no pre-adult stage [5]. Bath treatments are generally less effective because it is very Although direct measurement of individual life-spans is difficult, difficult to get a uniform concentration within the cage, so some laboratory studies and the fact that lice over-winter on wild salmon lice are not removed and concentrations can stress the fish [1,81]. [48] indicate individuals can live for over seven months. The loss of In addition, crowding stresses the fish, and it is very difficult to lice from fish in the laboratory cannot be assumed to be natural treat all cages on a site on the same day so lice can transfer to mortality as sea lice can easily escape from outflow pipes, and re-infest fish previously treated in other cages. However, in-feed where mortality occurs this might reflect suboptimal environmental treatments cannot be used when fish are not feeding. Furthermore, conditions (e.g. poor water quality). because they are systemic, it takes longer for levels in the fish to be reduced to those permissible for human consumption; which might delay harvest. The initial parasiticides used against sea lice were baths of the organophosphates trichlorvos and dichlorvos, now replaced by azamethiphos (also an organopho- sphate), cypermethrin and deltamethrin (permethrins) and hydro- gen peroxide. The in-feed treatments are the chitin synthesis inhibitors diflubenzuron and teflubenzuron and the most popular sea louse parasiticide emamectin benzoate. Resistance to organophosphates, permethrins and hydrogen peroxide has been recorded [82–84].
Increased average sea temperatures, whether due to annual variation or as predicted by climate change sce- narios for future decades (http://www.ipcc.ch), are likely to increase louse abundance on wild and farmed fish as a Figure I. The ten life-stages in the life-cycle of the sea louse Lepeophtheirus result of shorter generation times. In addition, they are salmonis. Free-living planktonic stages are shown in bold. likely to affect the geographical distribution of sea lice and Author's personaltheir wild hosts, potentially copy bringing new sea louse species and fecundity with temperature [10]. In addition, how the into contact with wild and farmed fish. Moreover, locally parasite–host interaction varies with temperature, as well increased maximum temperatures might stress sea lice as with the parasite and host species, remains unstudied, and/or their hosts. despite its implications for fish health management on Treatments that remove egg-bearing females during the salmon farms. winter or early spring could prevent the release of many Temperature-dependent life-cycle characteristics have larvae during the spring, leading to lower infestations on important implications for louse control on farms (Box 4). farmed and possibly wild salmon in the vicinity (Box 4). If a www.sciencedirect.com 478 Review TRENDS in Parasitology Vol.22 No.10 farm is exposed to infestations (from other farms or from Louse productivity wild fish) during the summer, parasiticide treatments are Most sea louse larval production in Ireland [22,23], Scot- required more frequently to interrupt the life cycle and land [24] and Norway [25] is currently from salmon farms, prevent exponential population growth. If a treatment because there are far more farmed than wild Atlantic affects only mobile stages, then repeat treatments are salmon in coastal waters and farmed salmon are present necessary when the chalimus stages moult to pre-adults, all year around. By contrast, wild salmonids migrate from perhaps only every one or two weeks at summer their natal freshwaters to the sea annually, and some temperatures. species move away from coastal waters during their mar- ine residence. In Norway, there are 100 times more farmed Intra- and interspecific competition than wild salmon, and escaped farm salmon have 10 times Competition for mates and avoidance interactions can more lice than wild salmon [26]. Thus, escaped fish could be affect the distribution of lice on the host. Adult male lice a significant reservoir of sea lice and could bring sea lice actively compete for and guard females before mating. into close proximity to wild fish. Significant numbers of Although the male transfers a spermatophore that blocks escaped farmed salmon also occur in the lower Bay of the female from further mating [12,13] for a time, females Fundy, Canada, and their louse burdens are similar to can mate again and polyandry is common [14]. Sperm levels on wild fish and on nearby farms [27], suggesting a storage reduces the need for mating at low parasite common infestation pool. More significant reservoirs of lice densities. occur on wild salmonids in the northern Pacific Ocean than The fact that the first infestations on farms are often in the Atlantic Ocean because more species of salmonids C. elongatus, later replaced by L. salmonis, which occur there and these fish are more abundant. This expo- thereafter remains the dominant species [15], suggests sure to infestation from wild fish is a concern for Pacific density-dependent inter-specific competition. Schram farms, but transfer of lice from farms to wild fish could also et al. [16] rejected competitive exclusion between these be locally significant [28,29]. species, but the intensity of infestation on the wild sea trout (Salmo trutta L.) that they analysed was low (< 0.04 Aggregation of lice on hosts lice gÀ1), so it is possible that no competition had occurred. On wild fish and during the early stages of farm infesta- Variation in the abundance of C. elongatus over time is tions, the frequency of occurrence of lice on the host popu- greater than might be expected from population growth lation is highly aggregated and the numbers of chalimus and mortality on wild sea trout [16] and on farmed Atlantic are fewer than of mobile stages [1,30], reflecting the longer salmon [17] and suggests that mobile stages might infest duration of the mobile life stage. This aggregated distribu- and leave their hosts. Although in the past L. salmonis has tion is typical of most parasites, with most hosts having few typically increased in abundance on farms despite or no sea lice. By contrast, when pathogenicity occurs on anti-parasite ‘bath’ treatments [17], C. elongatus farmed and wild fish, all or almost all hosts are infested, abundance is similar on farmed salmon in their first and the abundance of lice increases (Figure 2). Concomi- and second sea-years. This suggests re-infestation from tantly, the frequency distribution of parasites changes wild sources, which could explain the lack of benefit of from highly dispersed to normal [1], a pattern generally parasiticide treatments for C. elongatus on Scottish farms considered to indicate parasite-induced mortality [31]. [17]. Epizootics on wild sea trout smolts [1] and wild juvenile The prevalence and intensity (i.e. abundance on infected Pacific salmon [28] are characterized by the dominance of fish only) of sea lice generally increases with the age of wild chalimus stages. Laboratory infections typically have a Pacific salmon and with fish size. However, louse intensity normal distribution, probably related to more homogenous per unit area of fish surface does not increase with fish size experimental infestations, but also perhaps the result of [18,19], suggesting a maximum intensity of lice per host. lower genetic variation in farmed fish [18]. This could be a consequence of antagonistic interactions (interference competition) between sea lice jockeying for Abundance of pathogenic lice the best positions or competing for mates and/or the host The prevalence (% population infested) and the abundance being able to shed parasites by physically dislodging them. of lice on hosts increase in concert and show similar Immunological factors might be involved whereby an patterns for wild Pacific and Atlantic salmon and for sea increased host response offsets the increase in the sea trout in areas without salmon farms (Figure 2). Sea trout in louse population. For example, if the host developed sig- areas with salmon farms generally have more sea lice at all nificant immunity with age or duration of infestation, levels of prevalence, reflecting the higher proportions of decreased louse intensity would be expected, as occurs chalimi. Epizootics recorded on sea trout in Europe and for other ectoparasites [1]. One study found that repeated Pacific salmon in British Columbia tended to have over laboratory infectionsAuthor's of Atlantic salmon with L. salmonis personal60% prevalence and more copy than five lice per fish. Such louse do not predict later levels [20], but another suggested that levels have occurred on wild fish (Figure 2), and more prior louse infestation stimulates genetically based resis- heavily infested fish might not live to be sampled. Although tance of Atlantic salmon to L. salmonis [21]. Thus, before it this suggests that lice are pathogenic to more wild can be concluded that no long-term immune protection populations than previously appreciated, it should be develops in individual fish, such experiments need to be noted that Pacific salmon are less impacted by L. salmonis repeated at different louse intensities on fish of varying than Salmo spp., and larger fish can support more sea lice. age, size, genotype and physical condition. Levels of infection of < 0.1 mobile lice gÀ1 (i.e. ten lice on www.sciencedirect.com Review TRENDS in Parasitology Vol.22 No.10 479
Figure 2. Relationship of mean L. salmonis abundance to prevalence on samples from wild salmonids. Solid green circles, Pacific salmon; open blue circles, Atlantic salmon; blue triangles, sea trout outside areas with salmon farms; red triangles, sea trout within areas with salmon farms; open black diamonds, samples from epizootics on wild sea trout and sockeye salmon that represent known pathogenic infestations. Numbers include pre-adult, adult and chalimus stages, but the chalimus stages might have been underestimated in some samples. Sample sizes and host body size varied. The occurrence of some wild fish data within the area encompassed by the epizootic data, and the higher abundance on sea trout in areas near salmon farms, suggest that levels on wild fish above 60% prevalence and five lice per fish were pathogenic. The data and sources used to compile the figure are detailed in the Online Supplementary Material.
100 g fish) in experimental infections caused changes in infective planktonic copepodids. Plankton sampling in host physiology, biochemistry and immunology, in both the sea inlets in the mid-west of Ireland revealed that louse presence and absence of a host stress response [7,8]. Farm larvae, especially infective copepodids, are most abun- observations suggest that more than ten mobile lice per dant in shallow estuarine areas, ideal locations to inter- fish reduce the appetite of a 3–4 kg Atlantic salmon [32,33], cept migratory salmonids [42]. These studies revealed a and five per fish (0.05 to 0.1 mobile lice gÀ1) generally rapid decrease in sea louse nauplius concentrations away trigger treatment of smolts on farms. Thus, experimental from fish farms, but no such trends for copepodids. infections of individual fish, farm experience and patterns Sampling programmes in two Scottish lochs repeatedly across populations indicate that more than 5–10 lice per produced the highest concentrations of copepodids in fish (> 0.1 lice gÀ1) can or will become pathogenic. shallow water near the estuary mouth [43,44].Indeed, the highest concentrations of these larvae were caught Transmission with hand-nets by researchers wading along the shore, How copepodids increase their chances of intercepting a rather than from nets towed by boats. It thus seems that host has been one of the most challenging questions for L. salmonis larvae not only move vertically in the water researchers. The diversity of caligids, many specific to column, but are transported horizontally towards shal- certain species, genera or families of marine fish, demon- low waters, where salmonids are more abundant. An strates effective host-specific transmission. Microsatellite alternative hypothesis to explain estuarine concentra- [34] and mitochondrial [35] DNA analysis showed that tionsofcopepodidsisthatovigerouslicedetachfrom L. salmonis is a single population in the North Atlantic, salmonids that are migrating up rivers and the eggs but Atlantic and Pacific populations were distinct, survive and hatch in the estuary [42].Thishypothesis reflecting dispersal by their migratory hosts and plank- was proposed in part because the observed gradient of tonic larvae. Although genetics cannot discriminate decreasing concentrations of nauplii 2 km from a fish between populations of sea lice on wild and/or farmed fish farm was interpreted as requiring an alternative source [36–38], measures influenced by diet such as carbon–nitro- of louse infestation in the estuary. However, the gen stable isotope ratios [39], and by diet, environment and same study found no such gradient for copepodids, and genes such as elemental signatures [40], can do so. all other evidence suggests that larvae with a planktonic Furthermore, genetic analyses of other louse species have life span of several days disperse over much found sub-populationsAuthor's or cryptic species, illustrating thepersonalgreater distances than 2 kmcopy (see below). Furthermore, need for caution in generalizing between populations and L. salmonis do not fall off their host until in fresh water species [41]. for some days and their eggs do not hatch in fresh water [1]. Distribution of louse larvae Epizootics of sea lice on wild fish consist almost entirely Larval dispersal of chalimus stages [1,28] (Figure 2), indicating that the Lepeophtheirus salmonis do not find their hosts only in fish simultaneously encounter high concentrations of the estuaries. The presence of chalimi on wild salmon in the www.sciencedirect.com 480 Review TRENDS in Parasitology Vol.22 No.10 offshore Atlantic and Pacific oceans indicate they receive surface at night [1]. Some populations of scallop larvae low levels of L. salmonis infestation when away from have vertical migration adapted to local hydrographic the coast [9,46–48]. The typical development of conditions [55]. The evidence suggests that L. salmonis infestations on farmed salmon indicate that many larvae behaviour facilitates interception of salmonids migrating are available to re-infest their parent’s hosts, and plankton through estuaries. The fact that it survives much longer in sampling has shown that not all copepodids disperse away fresh water than C. elongatus [1], up to 14 days when from the cages [42]. A study on C. elongatus infesting attached to its host [58], could be an adaptation to survive haddock (Melanogrammus aeglefinus L.) suggested that on hosts that frequent brackish waters. louse larvae are distributed in a mid-water layer and Both active and passive mechanisms to aid host inter- intercept haddock that swim through this zone [1]. ception are probably involved. The larvae might have Salmonids typically feed at the surface in farm cages endogenous tidal rhythms, respond to sunlight, moonlight, and also come near the surface to feed in the wild. Thus salinity or water pressure, or detect turbulence associated vertical movement of sea louse larvae or their hosts could with high current velocities to stimulate upward swim- increase opportunity for parasite–host contact. ming and thus position themselves to be passively trans- Significant correlations between L. salmonis abundance ported in tidal currents as other larvae do on salmon in farms and on wild sea trout in Ireland has [7,55,56,59,60,61]. The larvae of many species concentrate been found up to 30 km from the farms [7,22]. Salmon on along pycnoclines [61], and vertical migration and reaction Norwegian farms that are > 10 km apart seem to have to salinity gradients is known for L. salmonis larvae [62]. fewer lice [49], as do pristine areas where farms In laboratory flumes, copepodid attachment to hosts was were absent [46]. A field and modelling study in British greatest in conditions of medium light (300 lux), full salin- Columbia found that larval dispersal and infestation on ity (35 parts per thousand) and low velocity (0.2 cm sÀ1) wild salmonids extends 30 km from a farm and that [63]. secondary production of lice from infested migrating wild Sea louse infestations have been observed to arrive in fish is detectable up to 75 km from the farm [29]. Sea louse pulses. This could be a passive consequence of lunar peri- larvae could disperse in a concentration gradient that odicity of the tides; the difference between spring and neap depends on tidal currents and prevailing wind patterns tides can result in concentration or dilution of sea louse [43,44,50]. larvae through changes of 25–30% of the tidal seawater Studies on other marine organisms that disperse in the volume in a bay. The risk of dilution could be offset by plankton have demonstrated passive transport of 2–23 km larvae concentrating in surface waters and against halo- in one 6 hour tide for seagrass [45], and mussel larvae clines. Further research into these mechanisms will enable can disperse an average of 20–30 km and have a population more spatially explicit estimates of the risk of infestation range of 60 km [51]. Decapod and cirripede crustaceans can on farmed and wild fish. invade new areas at a rate of 33–160 km per year [52]. From known larval survival data and dispersal distance it A transmission model for L. salmonis is possible to predict that louse larvae could disperse an Thefollowingprocesscouldexplainhowsealouselarvaeof average of 27 km (range 11–45 km) over 5–15 days [53]. L. salmonis are transported and concentrated into shallow Predicted average dispersal of sea louse larvae ranges from coastal and estuarine waters that salmonids frequent. 12 km (range 5–17 km) in low currents (5cmsÀ1)to Nauplii swim upwards during the day but do not actively 47 km (range 23–70 km) in higher currents (20 cm sÀ1) swim downwards. They are thus likely to concentrate in (B. Kinlan, personal communication). This suggests that surface waters. During the day, onshore winds generated sea louse larvae can typically disperse 10–50 km. However, by thermo-convection from warmer land drive surface the interaction between larval behaviour and local hydro- waters containing the sea lice towards the shore and graphic conditions can vary locally and could lead to larval towards estuaries (as these are further inland). Where retention within some areas [23]. Simple diffusion models fresh water lies on the surface, sea louse larvae can con- predicted dispersal of louse larvae from a farm in British gregate along the halocline. Thus larvae can concentrate Columbia and subsequent infestation of juvenile wild fish at the surface and/or the marine–freshwater interface, [29]. The species of sea lice infesting the farm was not which salmon smolts migrate through to enter ocean reported, but 53 of the 65 ovigerous lice on juvenile wild waters. Tidal currents increase in estuaries as the tidal fish were C. clemensi, a species found to infest returning volume is forced into a narrow channel. This increase in wild Pacific salmon in these coastal waters [54]. The dis- current velocity increases the likelihood of copepodids persion model could apply to this species or both it and being close to a potential host, although host attachment L. salmonis. The abundance of L. salmonis on wild fish has mightbemoredifficultinstrongercurrents[63].These also been linked to farms in the area [28]. options for the transmission model could be tested by Author's personalgiving particles a daily verticalcopy migration behaviour in Behaviour of Lepeophtheirus salmonis larvae a previously validated 3D hydrographic model that Larvae of many species, including crustaceans and mol- includes wind direction. A consequence of this transmis- luscs, migrate vertically with diel and tidal periodicities, sion mechanism is that the risk of infestation could be at with consequent transport into or out of estuaries and thus least as high near the shore and in estuaries as at an settlement in their preferred habitats [55–57]. Copepodids infested fish cage. This was the pattern observed on sal- of the copepod parasite Lernaeenicus sprattae (Sowerby. mon in experimental cages in Killary Harbour, Ireland 1806), and their juvenile fish hosts, concentrate at the sea [42]. www.sciencedirect.com Review TRENDS in Parasitology Vol.22 No.10 481
Future research Aberdeen), Per A. Kvenseth (Norsk Sjømatsenter, Bergen), Peter A. The most abundant and pathogenic sea lice on farmed fish Heuch (National Veterinary Institute, Oslo), Geoff Boxshall (Natural History Museum, London) and the anonymous referees that provided in Chile was recently found to be a species new to science, helpful comments on earlier drafts. and the commonest species in the North Atlantic, C. elon- gatus, has at least two genotypes. These findings empha- Appendix A. Supplementary data sise the need for more basic research on sea louse taxonomy Supplementary data associated with this article can be and natural hosts. found, in the online version, at doi:10.1016/ Research indicates roles for both the host immune j.pt.2006.08.006. response in reducing sea lice impacts and the parasite in suppressing such responses [8]. The former could reduce References louse development, fecundity and/or survival and be heri- 1 Costello, M.J. 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Short Communication
The global economic cost of sea lice to the salmonid farming industry
Mark J Costello
Leigh Marine Laboratory, University of Auckland, Warkworth, New Zealand
Keywords: aquaculture, Caligus, economic cost, chus spp., sea trout, Salmo trutta L., and charr, Lepeophtheirus, salmon, trout. Salvelinus alpinus (L.), from countries where sea lice have been reported to be a problem. Data were excluded for countries where sea lice have not been The economic cost of a problem may be the best reported as a significant problem, namely Australia, metric for prioritizing research and management Finland, France, Iceland, Japan, New Zealand and resources. Other metrics could be based on fish Sweden. To calculate costs per region, average costs welfare, and risks or impacts of parasiticides on the from Table 1 were used for UK (Scotland), most environment, farm staff or the consumer; but these recent cost for Norway, Norwegian cost for are not addressed here. Sea lice, ectoparasitic Faeroes, average of Atlantic Canada for all of copepod crustaceans, are the most damaging par- Canada and USA, and only the full cost for Chile. asite to the salmonid farming industry in both These costs were then multiplied by the 2006 Europe and the Americas (Costello 2006). Despite marine salmonid production to calculate costs per major research efforts over 30 years, as evident from country and globally (Table 2). Costs of sea lice over 800 research publications, they remain a control are reported in the original currency but persistent problem. The damage includes the converted to cost per kilogram of fish produced by impact on the fish and the environment, and public country. For comparative purposes, all values were perceptions of aquaculture (Costello 1993; Pike & converted to euros (€) in April 2008 to minimize Wadsworth1999; Costello, Grant, Davies, Cecchi- the effect of recent changes in the value of the ni, Papoutsoglou, Quigley & Saroglia 2001). US$. However, their economic cost has only been Ten estimates of costs because of sea lice were estimated at national or regional scales. Here, obtained from eight publications for Canada, Chile, published estimates of sea lice costs are presented Ireland, Norway and Scotland (Table 1). However, to stimulate better estimates, and provide an what costs the estimates included was only reported estimate of sea lice costs to the world salmonid in five publications. Whether costs varied between farming industry. Pacific and Atlantic Canada, and what they were for Estimated costs of sea lice control were obtained the USA, were not available. The lowest and highest from the literature (Table 1) and compared with estimates vary by a factor of 100 for full lice costs, the most recently available salmonid production and by 1000 where lower estimates only considered statistics (Table 2). The salmonid data used treatment expenses. These differences reflect the included marine production of Atlantic salmon, different costs between parasiticides and for the Salmo salar L., Pacific salmon species, Oncorhyn- same parasiticides between countries, and to a lesser extent price changes over time. Most estimates fell Correspondence Mark J Costello, University of Auckland, )1 Warkworth 0941, New Zealand within the range of €0.1–0.2 kg fish produced Ó 2009 The Author. (e-mail: [email protected]) annually. Journal compilation Ó 2009 Blackwell Publishing Ltd 115 Journal of Fish Diseases 2009, 32, 115–118 M J Costello Sea lice cost to salmonid farming
Table 1 Published estimates of the cost of sea lice to salmon farming including parasiticide use, effects on fish growth, and food conversion; except where not stated (*), or where stated to be for treatment costs only (**)
Lower Upper Cost (€ kg)1) (€ kg)1) Country Year Source
£0.153–0.230 kg)1 0.196 0.294 Scotland 2000 Rae (2002) US$0.3 kg)1 0.194 – Chile ? 1997 Carvajal et al. (1998) *1.503 Kr kg)1 0.185 – Norway 1997 Pike & Wadsworth (1999) *£0.134–0.269 kg)1 0.172 0.344 Scotland 1998 Pike & Wadsworth (1999) £0.123–0.261 kg)1 0.157 0.334 Scotland ? 1997 Sinnott (1998) *IR£0.08–0.10 kg)1 0.102 0.127 Ireland ? 2000 Anon (2003) *0.103 Kr kg)1 0.013 – Norway ? 1993 Maroni et al. (1994) Can$0.13–0.18 kg)1 0.082 0.114 Atlantic Canada ? 2000 Mustafa et al. (2001) **US$0.004–0.022 kg)1 0.003 0.014 Chile ? 2002 Bravo (2003) *Can$0.470 kg)1 – 0.298 Canada 1995 Pike & Wadsworth (1999)
Table 2 Estimated costs of sea lice control Value Cost sea Total based on 2006 salmonid production statis- Production (thousands lice control cost ) tics (FAO Fisheries and Aquaculture Infor- Country (tonnes) US$) € kg 1 € mation and Statistics Service 2008) Norway 689 970 2 649 930 0.19 131 094 300 Chile 647 445 3 839 713 0.19 123 014 550 United Kingdom 134 521 669 700 0.25 33 630 250 Canada, Pacific 70 178 392 333 0.10 7 017 800 Canada, Atlantic 47 880 267 675 0.10 4 788 000 Faeroes 18 574 92 878 0.19 3 529 060 Ireland 11 720 69 008 0.11 1 289 200 Maine, USA 9 401 37 510 0.10 940 100 Total 1 629 689 US$8 018 748 Median 0.19 305 303 260
The analysis assumed that sea lice control costs The absence of reports of sea lice problems in increased in proportion to production. In the past several countries merits study. It does not seem to five years, production increased in all countries be because of the absence of sea lice species. The except Faeroes, Ireland and USA where it salmon louse, Lepeophtheirus salmonis, occurs on significantly decreased. Because over 70% of world wild salmonids around Japan, and Caligus species production was from Norway and Chile, production occur worldwide. While L. salmonis is absent in the and sea lice control costs in these countries had the southern hemisphere, C. rogercresseyi has become greatest contribution to global costs. Multiplying the the pathogenic species on salmonid farms in Chile, sea lice costs by the FAO Fisheries and Aquaculture Caligus chiastos Lin and Ho on bluefin tuna, Information and Statistics Service (2008) salmonid Thunnus maccoyi (Castelnau), in South Australia production figures for 2006, indicated a total cost of (Hayward, Aiken & Nowak 2008), and C. epidem- €305 million, or US$480 million at present cur- icus Hewitt has been pathogenic to a range of wild rency exchange rates (Table 2). and farmed finfish species from Australia to south- While the sea lice control estimates and produc- east Asia. tion statistics used were the most recently found in Limited production may not provide the oppor- scientific publications, they may not reflect current tunity for sea lice epidemics to develop. This may costs. Because the basis of earlier and more recent explain the absence of a sea lice problem on estimates were not reported, it was not possible to salmonids in Denmark, France, Germany, Iceland, determine how sea lice control costs have changed New Zealand, Russia, Spain, Sweden and Turkey, over time. However, as profit margins get narrower where each countryÕs production was <8000 ton- because of increased competiveness as the industry nes p.a. in 2006 (FAO Fisheries and Aquaculture develops, fish-feed costs increase, and farms are Information and Statistics Service 2008). Salmonid under pressure to control lice to prevent spread to production in Australia and Finland is 20 000 and wild fish and other farms, it seems likely that sea lice 10 000 tonnes, respectively, but is in brackish control remains a significant limitation on farm waters which are less suitable for sea lice. In Ó 2009 The Author. profitability. addition, the short duration of the sea growing Journal compilation Ó 2009 Blackwell Publishing Ltd 116 Journal of Fish Diseases 2009, 32, 115–118 M J Costello Sea lice cost to salmonid farming
period in Japan (12 000 tonnes p.a.) prevents lice The most significant costs of sea lice where populations becoming significant on farms (Nagas- control is successful in preventing pathogenicity, are awa 2004). Alternatively, perhaps it is not total treatment costs, reduced fish growth, and reduced production, but the number and density of farm food conversion efficiency (Table 3). Further data sites that is significant in limiting the development to enable comparison of the effects of different of sea lice epidemics. Further research to under- control methods on fish growth and food conver- stand why lice are not a problem in some regions sion efficiency would enable more accurate esti- would be useful in developing methods to reduce mates of the costs of control options. Comparisons the risk of sea lice, and perhaps other pathogens, in between treatment options by Peddie (in Pike & sea cage farming in currently affected and unaf- Wadsworth 1999) in Scotland found an in-feed fected countries. treatment cost less than bath treatments because of It may be anticipated that there would be signif- the latter requiring more staff time and equipment, icant differences in control costs between countries and being more stressful to the fish. Using cleaner- (Table 1). Not only may staff and other operational wrasse was the next cheapest option after the in-feed costs vary between countries, but so can treatment treatments. However, the amount of wrasse could availability, and there may be significant differences have been halved and how their efficacy was in the details of how costs were calculated between determined was not stated; over time, wrasse are studies (Table 3). The costs in terms of compromised more efficacious in removing lice than bath treat- health, negative publicity from uses of parasiticides ments (Treasurer 2005; M. J. Costello, unpublished (Costello et al. 2001), and economic consequences of data). In contrast, Mustafa, Rankaduwa & Camp- cross-infection to wild fish, were not quantified in the bell (2001) compared two bath with one in-feed studies, and would be additional (Table 3). Indeed, if treatment and found the latter more expensive. It sea lice from farms have been significant in precip- must be appreciated that new parasiticides tend to itating the collapse of wild salmonid populations in be more expensive than established ones, especially Europe and Canada as recent data indicates (Ford & if the latter were widely used in other areas of Myers 2008), then the economic costs of sea lice are veterinary medicine. Furthermore, while there is a far greater than those presented here. close relationship between in-feed parasiticide costs
Table 3 A ranked importance of impacts of sea lice on the profitability of salmonid farming where control measures prevent pathogenicity
Rank Impacts Significance if sea lice control effective
1 Purchase costs of parasiticides 17–30% (Mustafa et al. 2001; Rae 2002) Purchase and maintenance costs of equipment of total lice control costs Staff time in research, management and control 2 Reduced fish growth 5–15% smaller weight (Sinnott 1998; M. J. Costello, unpublished data) 3 Reduced food conversion efficiency 5% more feed required (Sinnott 1998) 4 Reduced marketability because of disfigurement by lice 1% fish downgraded in Atlantic Canada (Mustafa et al. 2001) and up to 15% in Scotland (Michie 2001) 5 Stress and accidental mortalities because of parasiticide Only significant for bath treatments treatments and included in above costs 6 Negative publicity from the use of parasiticides that may While an estimate could be derived from leave residues in fish fillets, and/or are released into the price premium of organic salmon, the coastal environment such production is negligible globally Negative publicity and perhaps increased control required where farms may act as sources of sea lice that cause mass infestations (epizootics) that impact on wild fish populations of commercial, recreational, and/or cultural value 7 Losses because of secondary infections No evidence for significant transmission of pathogens by sea lice, and if controlled, damage to host skin will be minimized 8 More expensive farming practices Preventative measures also minimize transmission of other pathogens, so this is considered a cost of business 9 Fish mortality <1% (as non-pathogenic) Ó 2009 The Author. Journal compilation Ó 2009 Blackwell Publishing Ltd 117 Journal of Fish Diseases 2009, 32, 115–118 M J Costello Sea lice cost to salmonid farming
and fish weight, that for bath treatments depends Carvajal J., Gonzalez L. & Nascimento M. (1998) Native sea lice on sea-cage size, which has a more variable (Copepoda: Caligidae) infestation of salmonids reared in net- relationship to fish weight. Thus, the choice of pen systems in southern Chile. Aquaculture 166, 241–246. the most cost-effective control method must be Costello M.J. (1993) Review of methods to control sea lice (Caligidae: Crustacea) infestations on salmon (Salmo salar) calculated in the context of the farm operational farms. In: Pathogens of Wild and Farmed Fish: Sea Lice (ed. by costs, and costs of methods available to the farm at G.A. Boxshall & D. Defaye), pp. 219–252. Ellis Horwood, the time. Chichester. There are several species of sea lice in most Costello M.J. (2006) Ecology of sea lice parasitic on farmed and countries farming salmonids, and they have several wild fish. Trends in Parasitology 22, 475–483. wild hosts. Thus a reservoir of lice will always be Costello M.J., Grant A., Davies I.M., Cecchini S., Papoutsoglou present around the farms. As new species are S., Quigley D. & Saroglia M. (2001) The control of chemicals cultured and production increases, it may be only a used in aquaculture in Europe. Journal of Applied Ichthyology 17, 173–180. matter of time before sea lice similarly infect them. Research into the ecology of other sea lice species, FAO Fisheries and Aquaculture Information and Statistics Ser- vice (2008) Aquaculture Production 1950–2006. FISHSTAT and understanding of how epidemics develop and Plus-Universal Software for Fishery Statistical Time Series [On- persist, will enable the development of strategies to line or CD-ROM]. Food and Agriculture Organization of the reduce the risk of sea lice impacting on current and United Nations. Available at: http://www.fao.org/fi/statist/ emerging farmed finfish. Research and management FISOFT/FISHPLUS.asp (last accessed on 14 April 2008). measures to avoid farm infection from other farms Ford J.S. & Myers R.A. (2008) A global assessment of salmon and wild fish, and cultured fish that are lice resistant aquaculture impacts on wild salmonids. PLoS Biology 6, e33, doi:10.1371/journal.pbio.0060033. (e.g. on which lice cannot reproduce), whether mediated by genetic breeding or diet, may be the Hayward C.J., Aiken H.M. & Nowak B.F. (2008) An epizootic of Caligus chiastos on farmed southern bluefin tuna Thunnus best strategies to reduce annual costs to the maccoyi off South Australia. Diseases of Aquatic Organisms 79, industry. 57–63. In 2006, total salmonid marine production was Maroni K., Steinshylla K. & Willumsen F.W. (1994) Optimal 1.7 million tonnes worth US$8.4 billion (FAO lokalisering, strukturering og drift av matfiskanlegg. Rapport Fisheries and Aquaculture Information and Statis- 193, KPMG (Akva Instituttet), Trondheim. In Norwegian, p. tics Service 2008). Available data indicates sea lice 73. In: Hevrøy E.M. Boxaspen K., Oppedal F., Taranger G.L., )1 Holm J.C. 2003. The effect of artificial light treatment and cost from €0.1 to €0.2 kg of fish (Table 1). depth on the infestation of the sea louse Lepeophtheirus sal- However, without such treatment measures, sea lice monis on Atlantic salmon (Salmo salar L.) culture. Aquaculture would cost the industry at least four times more 220, 1–14. (Mustafa et al. 2001), and probably increase to Michie I. (2001) Causes of downgrading in the salmon farming levels such as to cause significant direct and indirect industry. Kestin, S.C. and Warris, P.D., editors Farmed fish mortality to stock. Regional estimates for the cost of quality. Fishing News Books, Oxford, pp. 129–136. sea lice ranged from 4% of production value for Mustafa A., Rankaduwa W. & Campbell P. 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(1998) Sea lice – watch out for the hidden costs. Fish References Farmer 21(3), 45–46. Anon. (2003) Salmon Farming: Towards an Integrated Pest Treasurer J.W. (2005) Cleaner fish: a natural approach to the Management Strategy for Sea Lice. Report on the international control of sea lice on farmed fish. Veterinary Bulletin 75, 17–29. conference on sea lice management, Aberdeen, Scotland, Received: 14 April 2008 Caligus No.7, 6. Revision revised: 10 October 2008 Bravo S. (2003) Sea lice in Chilean salmon farms. Bulletin of the Accepted: 23 October 2008 European Association of Fish Pathologists 23, 197–200. Ó 2009 The Author. Journal compilation Ó 2009 Blackwell Publishing Ltd 118