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Sea lice is the term generally used for species of copepods within the order Siphonostomatoida, family Caligidae. There are 36 genera within this family which include approximately 42 Lepeophtheirus and 300 Caligus species[1]. Sea lice are ectoparasites (external parasites) feeding on the mucus, epidermal tissue, and blood of host marine fish. L. salmonis and various Caligus species are adapted to saltwater and are major ectoparasites of farmed Atlantic salmon. Several antiparasitic drugs have been developed for control purposes. Since L. salmonis is the major sea lice of concern and has the most known about its biology and interactions with its salmon host, this review will focus on this species. Caligus rogercresseyi has become a major parasite of concern on salmon farms in Chile[2] and studies are underway to gain a better understanding of the parasite and the host-parasite interactions. Recent evidence is also emerging that L. salmonis in the Atlantic has sufficient genetic differences from L. salmonis from the Pacific, suggesting that Atlantic and Pacific L. salmonis may have independently co-evolved with Atlantic and Pacific salmonids, respectively[3]. Other distinct differences, such as lower pathogenicity of Pacific L. salmonis, higher tolerance for reduced salinity, as well as the ability to develop part of its life cycle on the three-spined stickleback (Gasterosteus aculeatus L.)[4], may have evolved separately as well.

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Sea Lice
Male and female Lepeophtheiris salmonis
Scientific classification
Kingdom:
Animalia
Phylum:
Arthropoda
Subphylum:
Crustacea
Class:
Maxillopoda
Subclass:
Copepoda
Superorder:
Podoplea
Order:
Siphonostomatoida
Families

Caligidae

Diversity
36 genera, c. 500 species




Diversity and hosts: Sea lice on wild fish

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Most of the biology of sea lice, other than the early morphological studies, are based on laboratory studies to solve problems associated with sea lice infecting fish on salmon farms. Information on sea lice biology and life cycles with respect to wild fish is unfortunately sparse. Many sea lice are very specific with regards to host, particularly L. salmonis which has high specificity for Atlantic salmon (Salmo salar). L. salmonis can parasitize other salmonids to varying degrees, including brown trout (sea trout: Salmo trutta), and some Pacific Oncorhynchus spp. including rainbow trout or steelhead (O. mykiss) and to some extent Chinook salmon (O. tshawytscha). Coho, chum, and pink salmon (O. kisutch, O. keta, and O. gorbuscha, respectively) mount strong tissue responses to attaching L. salmonis, which lead to rejection within the first week of infection[5]. Pacific L. salmonis can also develop, but not complete, its full life cycle on the three-spined stickleback (Gasterosteus aculeatus L.)[4], which is not seen with Atlantic L. salmonis.

How planktonic larvae disperse and find a new host is still not completely known. Temperature, light and currents are major factors and survival depends on salinity above 25 ppt[6] [7][8]. It has been hypothesized that L. salmonis copepodids migrating upwards towards light and salmon smolt moving downwards at daybreak facilitate in finding a host[9]. Several studies have examined copepodid populations in intertidal zones and showed that planktonic stages can be transported many kilometers from their source[10].

The source of sea lice infections when salmon return from freshwater has always been a mystery. Sea lice die and fall off anadromous fish such as salmonids when they return to freshwater. Salmon go upstream in the fall to reproduce and the smolt do not return to saltwater until the next spring. It is possible that sea lice survive on fish that remain in the estuaries or that they transfer to an as yet unknown alternate host to spend the winter. Nonetheless, smolt get infected with sea lice larvae, or even possibly adults, when they enter the estuaries in the spring. It is also not known how sea lice distribute between fish in the wild. Adult stages of Lepeophtheirus spp. can transfer under laboratory conditions, but the frequency is low. Caligus spp. transfer quite readily and between different species of fish.


Morphology

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Lepeophtheirus spp. tend to be approximately twice the size of most Caligus spp. The body consists of 4 regions: cephalothorax, fourth leg-bearing segment, genital complex, and abdomen[11]. The cephalothorax forms a broad shield that includes all of the body segments up to the third-leg bearing segment. It acts like a suction cup in holding the louse on the fish. All species have mouth parts shaped as a siphon or oral cone (characteristic of the Siphonostomatoida). The second antennae and oral appendages are modified to assist in holding the parasite on the fish. The second antenna is also used by males to grasp the female during copulation[12]. The adult females are always much larger than males and develop a very large genital complex which in many species makes up the majority of the body mass. Two egg strings of 500 to 1000 eggs (L. salmonis) that darken with maturation are approximately the same length as the female’s body. One female can release 6-11 pairs of egg strings in a lifetime of approximately 7 months[13][14][15].


Development

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Sea lice have both free swimming (planktonic) and parasitic life stages. All stages are separated by moults[16][17][18][19]). The development rate for L. salmonis from egg to adult varies from 17 to 72 days depending on temperature. The life cycle of L. salmonis is shown in the figure; the sketches of the stages are from Schram[18].

Eggs hatch into nauplius I which moult to a second naupliar stage; both naupliar stages are non-feeding, depending on yolk reserves, and adapted for swimming. The copepodid stage searches for an appropriate host, likely by chemo- and mechanosensory clues. Currents, salinity, light, and other factors also will assist copepodids in finding a host Cite error: A <ref> tag is missing the closing </ref> (see the help page).[7]. Once in contact with a host fish, they develop into chalimus I which attaches to the skin of the host by a unique frontal filament and moult through 4 stages. There are differences in the timing, method of production and the physical structure of the frontal filament between different species of sea lice. Pre-adult and adult stages are mobile on the fish and, in some cases, can move between host fish. Adult females, being larger, occupy relatively flat body surfaces on the posterior ventral and dorsal midlines and may actually out-compete pre-adults and males at these sites[20]. The smaller males and pre-adult males and females settle in concave depressions on the body, such as in the head region.


Feeding Habits

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The naupliar and copepodid stages are non-feeding and live on endogenous food stores. Chalimus stages have a developed gastrointestinal tract and feed on mucus within range of their attachment. Pre-adult and adult sea lice, especially gravid females are aggressive feeders and begin to feed on skin and blood, in addition to mucus. Blood is often seen in the digestive tract. It is not known whether sea lice are vectors of disease, but they can be carriers of bacteria and viruses obtained from tissues of contaminated fish[21].


Disease

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Pathology

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Gravid female Lepeophtheiris salmonis on Atlantic salmon, Salmo salar

Sea lice cause physical and enzymatic damage at their sites of attachment and feeding which results in abrasion-like lesions that vary in their nature and severity depending upon a number of factors. These include host species, age and general health of the fish. Stressed fish are particularly prone to infestation. Sea lice infection itself causes a generalized chronic stress response in fish since feeding and attachment cause changes in the mucus consistency and damage the epithelium resulting in loss of blood and fluids, electrolyte changes, and cortisol release. This can decrease salmon immune responses and make them susceptible to other diseases and reduces growth and performance.

The degree of damage is also dependent on the species of sea lice, the developmental stages that are present, and the number of sea lice on a fish. There is little evidence of host tissue responses in Atlantic salmon at the sites of feeding and attachment, regardless of the development stage. In contrast, coho and pink salmon show strong tissue responses to L. salmonis characterized by epithelial hyperplasia and inflammation. This results in rejection of the parasite within the first week of infection in these species of salmonids[5]. Heavy infections of Atlantic salmon by L. salmonis can lead to deep lesions, particularly on the head region, even exposing the skull. These are rarely seen on fish farms anymore because of good therapeutic control measures being in place.


Wild - farmed fish interactions

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There is reported concern that sea lice flourishing on salmon farms can spread to nearby wild juvenile salmon and devastate these populations.[22] Sea trout populations in recent years have seriously declined due to infestation by sea lice from salmon farms.[23] Several scientific studies have suggested that caged farmed salmon harbour lice to a degree that can destroy surrounding wild salmon populations[24]. Other studies have shown that lice from farmed fish have relatively no effect on wild fish if good husbandry and adequate control measures are carried out[25] (also, see section: Control on salmon farms). Further studies to establish wild-farmed fish interactions are on-going, particularly in Canada, Scotland, Ireland, and Norway. A reference manual with protocol and guidelines for studying wild/cultured fish interactions with sea lice has been published[26].


Fish Farming

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Control on salmon farms

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This has been well reviewed by McVicar[27] and Costello[15]. Integrated pest management programs for sea lice are instituted or recommended in a number of countries, including Canada[28][29], Norway[25], Scotland[30], and Ireland[31]. Identification of epidemiological factors as potential risk factors for sea lice abundance[32] with effective sea lice monitoring programs have been shown to effectively reduce sea lice levels on salmon farms[33].


Natural predators

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Cleaner fish, including five species of wrasse (Labridae), are used on fish farms in Europe, particularly to remove larger lice such as gravid females[34]. They are not used in other fish farming regions, such as Atlantic Canada, since they are not indigenous to these areas, and have limited efficacy.


Husbandry

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Good husbandry techniques include fallowing, removal of dead and sick fish, prevention of net fouling, etc. Bay management plans are in place in most fish farming regions to keep sea lice below a level that could lead to health concerns on the farm or affect wild fish in surrounding waters. These include separation of year classes, counting and recording of sea lice on a prescribed basis, use of parasiticides when sea lice counts increase, monitoring for resistance.


Salmon breeding

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Early findings showed genetic variation in the susceptibility of Atlantic salmon to Caligus elongatus[35]. Research then began to identify trait markers[36] and recent studies have shown that susceptibility of Atlantic salmon to L. salmonis can be identified to specific families and that there is a link between MHC Class II and susceptibility to lice[37].


Drugs and Vaccines

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The range of therapeutants for farmed fish has been very limited, largely due to environmental concerns. However, all drugs used have been thoroughly assessed for their environmental impact and risks[38][39]. The parasiticides are classified into bath and in-feed treatments as follows:


Bath Treatments:

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There are both advantages and disadvantages to using bath treatments. Bath treatments are more difficult and need more manpower to administer, requiring skirts or tarpaulins to be placed around the cages to contain the drug. Prevention of reinfection is a challenge since it is practically impossible to treat an entire bay in a short time period. Since the volume of water is imprecise, the required concentration is not guaranteed. Crowding of fish to reduce the volume of drug can also stress the fish. Recent use of well-boats containing the drugs has reduced both the concentration and environmental concerns, although transferring fish to the well boat and back to the cage can be stressful. The major advantage to bath treatments is that all the fish will be treated equally, in contrast to in-feed treatments where amount of drug ingested can vary due to a number of reasons.


Organophosphates

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Organophosphates are acetylcholinesterase inhibitors and cause excitatory paralysis leading to death of sea lice when given as a bath treatment. Dichlorvos was used for many years in Europe and later replaced by azamethiphos, the active ingredient in Salmosan, which is safer for operators to handle[40]. Azamethiphos is water-soluble and broken down relatively quickly in the environment. Resistance to organophosphates began to develop in Norway in the mid 1990’s, apparently due to acetylcholinesterases being altered due to mutation[41]. Use has declined considerably with the introduction of SLICE, emamectin benzoate.


Pyrethroids

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Pyrethroids are direct stimulators of sodium channels in neuronal cells, inducing rapid depolarization and spastic paralysis leading to death. The effect is specific to the parasite since the drugs used are only slowly absorbed by the host and rapidly metabolized once absorbed. Cypermethrin (Excis, Betamax) and deltamethrin (Alphamax) are the two pyrethroids commonly used to control sea lice. Resistance to pyrethroids has been reported in Norway and appears to be due to a mutation leading to a structural change in the sodium channel which prevents pyrethroids from activating the channel[42]. Use of deltamethrin has been increasing as an alternate treatment with the rise in resistance observed with emamectin benzoate.


Topical Disinfectants

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Bathing fish with hydrogen peroxide (350-500 mg/L for 20 min) will remove mobile sea lice from fish. It is environmentally friendly since H2O2 dissociates to water and oxygen, but can be toxic to fish, depending on water temperature, as well as to operators[43]. It appears to knock the sea lice off the fish, leaving them capable of reattaching to other fish and reinitiating an infection.


In-feed Treatments:

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In-feed treatments are easier to administer and pose less environmental risk than bath treatments. Feed is usually coated with the drug and drug distribution to the parasite is dependent on the pharmacokinetics of the drug getting in sufficient quantity to the parasite. The drugs have high selective toxicity for the parasite, are quite lipid soluble so that there is sufficient drug to act for approximately 2 months, and any unmetabolized drug is excreted so slowly that there are little to no environmental concerns.


Avermectins

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Avermectins belong to the family of macrocyclic lactones and are the major drugs used as in-feed treatments to kill sea lice. The first avermectin used was ivermectin, but was toxic to fish, causing sedation and central nervous system depression due to the drug’s ability to cross the blood brain barrier. Emamectin benzoate, which is the active agent in the formulation SLICE[44], has been used since 1999 and has no side effects on fish. It is administered at 50µg/kg/day for 7 days and is effective for two months, killing both chalimus and mobile stages. Withdrawal times vary with jurisdiction from zero in Canada to 175 degree days in Norway. Avermectins act by opening glutamate-gated chloride channels in arthropod neuromuscular tissues, causing hyperpolarization and flaccid paralysis leading to death. Resistance has been noted in Chalimus rogercresseyi in Chile and L. salmonis on North Atlantic fish farms. The resistance to likely due to prolonged use of the drug leading to up-regulation of P-glycoprotein[45], similar to what has been seen in nematode resistance to macrocyclic lactones[46].


Growth Regulators

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Teflubenzuron, the active agent in the formulation Calicide[47], is a chitin synthesis inhibitor and prevents moulting. It thus prevents further development of larval stages of sea lice, but has no effect on adults. It has been used only sparingly in sea lice control, largely due to concerns that it may affect other crustaceans in the sea that may moult, although this has not been shown at the concentrations recommended[38]. The drug is no longer available due to the production factory burning down.


Vaccines:

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A number of studies are underway to examine various antigens, particularly from the gastrointestinal tract and reproductive endocrine pathways, as vaccine targets, but no vaccine against sea lice has been reported to date.


Other points of interest:

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Branchiurans, family Argulidae, order Arguloida are known as fish lice and parasitize fish in freshwater.


References

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  1. ^ Walter, T.C., Boxshall, G. (Eds) 2009. “World Copepoda database”. Accessed through the World Register of Marine Species. http://www.marinespecies.org/aphia.php?p=taxdetails&id=349547 on 2009-08-17
  2. ^ Bravo, S. 2003. “Sea lice in Chilean salmon farms”. Bull. Eur. Ass. Fish Pathol. 23, 197–200.
  3. ^ Yazawa, R., Yasuike, M., Leong, J., von Schalburg, K.R., Cooper, G.A., Beetz-Sargent, M., Robb, A., Davidson, W.S., Jones, S.R., and Koop, B.F. 2008. “EST and mitochondrial DNA sequences support a distinct Pacific form of salmon louse, Lepeophtheirus salmonis”. Mar. Biotechnol. (NY) 10, 741-749. doi:10.1007/s10126-008-9112-y pmid:18574633
  4. ^ a b Jones, S.R.M., Kim, E. & Dawe, S. 2006. “Experimental infections with Lepeophtheirus salmonis (Krøyer) on three-spine sticklebacks, Gasterosteus aculeatus L., and juvenile Pacific salmon, Oncorhynchus spp.”. J. Fish Dis. 29, 489-495. DOI: 10.1111/j.1365-2761.2006.00742
  5. ^ a b Wagner, G.N., Fast, M.D. & Johnson, S.C. 2008. “Physiology and immunology of Lepeophtheirus salmonis infections of salmonids”. Trends Parasitol. 24, 176-183
  6. ^ Costelloe, M., Costelloe, J., O’Donohoe, G. Coghlan, N.J., Oonk, M., & van der Heijden, Y. 1998. “Planktonic distribution of sea lice larvae Lepeophtheirus salmonis, in Killary harbor, west coast of Ireland. J. Mar. Biol. Assoc. UK 78, 853-874
  7. ^ a b Genna, R.L., Mordue, W., Pike, A.W., & Mordue-Luntz, A.J. 2005. “Light intensity, salinity, and host velocity influence presettlement intensity and distribution on hosts by copepodids of sea lice, Lepeophtheirus salmonis”. Can. J. Fish. Aquat. Sci. 62, 2675-2682
  8. ^ Brooks, K.M. 2005. “The effects of water temperature, salinity, and currents on the survival and distribution of the infective copepodid stage of sea lice (Lepeophtheirus salmonis) originating on Atlantic salmon farms in the Broughton Archipelago of British Columbia, Canada”. Rev. Fish. Sci. 13, 177-204
  9. ^ Heuch, P.A., Parsons, A., & Boxaspen, K. 1995. “Diel vertical migration: A possible host finding mechanism in salmon lice (Lepeophtheirus salmonis) copepodid?” Can. J. Fish. Aquat. Sci. 52, 681-689
  10. ^ McKibben, M.A. & Hay, D.W. 2004. "Distributions of planktonic sea lice larvae Lepeophtheirus salmonis in the inter-tidal zone in Loch Torrindon, western Scotland in relation to salmon farm production cycles". Aquacult. Res. 35, 742–750
  11. ^ Johnson, S.C. & Albright, L.J. 1991. “The developmental stages of Lepeophtheirus salmonis (Krøyer, 1837) (Copepoda: Caligidae)”. Can. J. Zool. 69, 929-950
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  16. ^ Anstensrud, M. 1990. “ Moulting and mating in Lepeophtheirus pectoralis (Copepoda: Caligidae)”. J. Mar. Biol. Ass. U.K. 70, 269-281
  17. ^ Johnson, S.C. & Albright, L.J. 1991. “The developmental stages of Lepeophtheirus salmonis (Krøyer, 1837) (Copepoda: Caligidae)”. Can. J. Zool. 69, 929-950
  18. ^ a b Schram, T.A. 1993. “Supplementary description of the developmental stages of Lepeophtheirus salmonis (Krøyer, 1837) (Copepoda: Caligidae)”. In Pathogens of Wild and Farmed Fish: Sea Lice (eds. G.A. Boxshall, & D. Defaye), Ellis Horwood, Chichester, UK
  19. ^ Pike, A.W. & Wadsworth, S.L. 2000. “Sealice on salmonids: their biology and control”. Adv. Parasitol. 44, 233-337
  20. ^ Todd, C.D., Walker, A.M., Hoyle, J.E., Northcott, S.J., Walker, A.F., & Ritchie, M.G. 2000. “Infestations of wild adult Atlantic salmon (Salmo salar L.) by the ectoparasitic copepod sea louse Lepeophtheirus salmonis (Krøyer): prevalence, intensity and the spatial distribution of males and females on the host fish”. Hydrobiologia 429, 181-196
  21. ^ Nylund, A., Bjørknes, B., & Wallace, C. 1991. “Lepeophtheirus salmonis – a possible vector in the spread of diseases on salmonids. Bull. Europ. Assoc. Fish Pathol. 11, 213-216
  22. ^ Martin Krkosek, Jennifer S. Ford, Alexandra Morton, Subhash Lele, Ransom A. Myers, and Mark A. Lewis (14 December 2007), "Declining Wild Salmon Populations in Relation to Parasites from Farm Salmon". Science 318 (5857), 1772.
  23. ^ Clover, Charles (2004). The End of the Line: How Overfishing is Changing the World and What We Eat. London: Ebury Press. ISBN 0-09-189780-7.
  24. ^ Krkosek, M., Lewis, M.A., Morton, A., Frazer, L.N. & Volpe, J. 2006. "Epizootics of wild fish induced by farm fish". Proc. Natl. Acad. Sci. USA 103, 15506-15510
  25. ^ a b Heuch, P.A. Bjørn, P.A., Finstad, B., Holst, J.C., Asplin, L. & Nilsen, F. 2005. “A review of The Norwegian Action Plan Against Salmon Lice on Salmonids: the effect on wild salmonids”. Aquaculture 246, 79-92
  26. ^ http://www.pacificsalmonforum.ca/wild/index.php, on 2009-09-17
  27. ^ McVicar, A.H. 2004. “Management actions in relation to the controversay about salmon lice infections in fish farms as a hazard to wild salmonid populations”. Aquacult. Res. 35, 751-758
  28. ^ http://www.hc-sc.gc.ca/cps-spc/pubs/pest/_fact-fiche/lice-pou/index-eng.php on 2009-09-11
  29. ^ http://www.al.gov.bc.ca/ahc/fish_health/SL%20Mgmnt%20Strat%202007%202008%20Final.pdf on 2009-09-11
  30. ^ Rosie, A.J. and Singleton, P.T.R. 2002. “Discharge consents in Scotland”. Pest Manag. Sci. 58, pp. 616–621
  31. ^ Grist B. 2002. “The regulatory system for aquaculture in the Republic of Ireland”. Pest Manag. Sci. 58: 609–615
  32. ^ Revie, C.W., Getinby, G., Treasurer, J.W. & Wallace, C. 2003. "Identifying epidemiological factors affecting sea lice Lepeophtheirus salmonis abundance on Scottish salmon farms using general linear models". Dis. Aquat. Org. 57, 85-95
  33. ^ Saksida, S., Karreman, G.A., Constantine, J., & Donald, A. 2007. "Differences in Lepeophtheirus salmonis abundance levels on Atlantic salmon farms in the Broughton Archipelago, British Columbia, Canada". J. Fish Dis. 30, 357-366
  34. ^ Treasurer, J.W. 2002. “A review of potential pathogens of sea lice and the application of cleaner fish in biological control”. Pest Manag. Sci. 58, 546-558
  35. ^ Mustafa, A. & MacKinnon, B.M. 1999. "Genetic variation in susceptibility of Atlantic salmon to the sea louse Caligus elongatus Nordmann 1882". Can. J. Zool. 77, 1332-1335
  36. ^ Jones, C.S., Lockyer, A.E., Verspoor, E., Secombes, C.J., & Noble, L.R. 2002. “Towards selective breeding of Atlantic salmon for sea louse resistance: approaches to identify trait markers”. Pest Manag. Sci. 58, 559-568
  37. ^ Glover, K.A., Grimholt, U., Bakke, H.G., Nilsen, F., Storset, A. &, Skaala, Ø. 2007. “Major histocompatibility complex (MHC) variation and susceptibility to the sea louse Lepeophtheirus salmonis in Atlantic salmon Salmo salar”. Dis. Aquat. Org. 76, 57-66
  38. ^ a b Burrage, L.E. 2003. “Chemical use in marine finfish aquaculture in Canada: A review of current practices and possible environmental effects”. Can. Tech. Rep. Fish. Aquat. Sci. 2450, 97-131
  39. ^ Haya, K., Burrage, L.E., Davies, I.M., & Ervik, E. 2005. “A review and assessment of environmental risk of chemicals used for the treatment of sea lice infestations of cultured salmon”. Hdb. Env. Chem. 5, Part M, 305-340
  40. ^ Denholm, I., Devine, G.J., Horsberg, T.E., Sevatdal, S., Fallang, A., Nolan, D.V., & Powell, R. 2002. “Analysis and management of resistance to chemotherapeutants in salmon lice Lepeophtheirus salmonis (Copepoda: Caligidae)”. Pest Manag. Sci. 58, 528-536
  41. ^ Fallang, A., Ramsay, J.M., Sevatdal, S., Burka, J.F., Jewess, P., Hammell, K.L., & Horsberg, T.E. 2004. “Evidence for occurrence of an organophosphate-resistant type of acetylcholinesterase in strains of sea lice (Lepeophtheirus salmonis Krøyer)”. Pest Manag. Sci. 60, 1163-1170
  42. ^ Fallang, A., Denholm, I., Horsberg, T.E., & Williamson, M.S. 2005. “Novel point mutation in the sodium channel gene of pyrethroid-resistant sea lice Lepeophtheirus salmonis (Crustacea: Copepoda)”. Dis. Aquat. Org. 65, 129-136
  43. ^ Grant, A.N. 2002. “Medicines for sea lice”. Pest Manag. Sci. 58, 521-527
  44. ^ Schering-Plough Animal Health: http://www.spaquaculture.com/default.aspx?pageid=545 on 2009-09-11
  45. ^ Tribble, N.D., Burka, J.F., Kibenge, F.S.B., & Wright, G.M. 2008. "Identification and localization of a putative ATP-binding cassette transporter in sea lice (Lepeophtheirus salmonis) and host Atlantic salmon (Salmo salar)". Parasitol. 135, 243-255
  46. ^ Lespine, A., Alvinerie, M., Vercruysse, J., Prichard, R.K., & Geldhof, P. 2008. “ABC transporter modulation: a strategy to enhance the activity of macrocyclic lactone anthelmintics”. Trends Parasit. 24, 293-298
  47. ^ EMEA 1999. “Teflubenzuron, summary report” http://www.emea.europa.eu/pdfs/vet/mrls/054799en.pdf on 2009-09-11


Category:Fish diseases Category:Veterinary parasitology Category:Aquaculture Category:Crustaceans

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