{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,29]],"date-time":"2026-01-29T13:30:52Z","timestamp":1769693452879,"version":"3.49.0"},"reference-count":50,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2023,9,10]],"date-time":"2023-09-10T00:00:00Z","timestamp":1694304000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Fishes"],"abstract":"<jats:p>Salmon lice are one of the biggest challenges to sustainable salmonid aquaculture. The species display high evolutionary potential, which is evident by its development of resistance to numerous chemical compounds used for delousing. In response to this, salmon farms now use non-chemical delousing methods to minimize the damage done by salmon lice, including heavy reliance on cleaner fish. Anecdotal reports from farmers and fish health personnel in areas where cleaner fish are used have suggested that salmon lice are becoming less pigmented, potentially making them harder for cleaner fish to visually detect. This experiment investigated changes in the pigmentation of salmon lice in relation to the use of cleaner fish, louse stage and sex, temperature, preferred salmon swimming depth, daylength, and salinity. Salmon lice were sampled from snorkel cages on a commercial salmon farm where three cages were stocked with farmed lumpfish and ballan wrasse, and three cages were without cleaner fish. Water temperature, salinity, and depth were recorded using a conductivity, temperature, and depth recorder. Pigmentation was measured via photographic analysis of individual lice. Although louse pigmentation varied considerably throughout the experiment, using cleaner fish throughout a single production cycle did not reduce average louse pigmentation compared to control cages. On average, male lice were significantly darker pigmented than females, but otherwise there were no patterns in louse pigmentation in relation to life stage, salinity, temperature, or daylength. Salmon lice exhibit a high degree of evolvability and have become resistant to every chemical removal treatment developed thus far. The present data suggest that, with the densities and species of cleaner fish commonly used in commercial salmon production, there is not strong directional selection on louse pigmentation. Lice, at least with regard to visual appearance, are not likely to adapt in a way which reduces cleaner fish efficacy anytime soon.<\/jats:p>","DOI":"10.3390\/fishes8090455","type":"journal-article","created":{"date-parts":[[2023,9,11]],"date-time":"2023-09-11T09:11:18Z","timestamp":1694423478000},"page":"455","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Cleaner Fish Do Not Impact the Pigmentation of Salmon Lice (Lepeophtheirus salmonis) in Commercial Aquaculture Cages"],"prefix":"10.3390","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0077-8077","authenticated-orcid":false,"given":"Albert Kjartan Dagbjartarson","family":"Imsland","sequence":"first","affiliation":[{"name":"Akvaplan-niva Iceland Office, Akralind 6, 201 K\u00f3pavogur, Iceland"},{"name":"Department of Biological Sciences, University of Bergen, High Technology Centre, 5020 Bergen, Norway"}]},{"given":"Jon Petter","family":"Berg","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, University of Bergen, High Technology Centre, 5020 Bergen, Norway"}]},{"given":"Velimir","family":"Nola","sequence":"additional","affiliation":[{"name":"Institute of Marine Research, Matre Research Station, 5984 Matredal, Norway"}]},{"given":"Lena","family":"Geitung","sequence":"additional","affiliation":[{"name":"Institute of Marine Research, Matre Research Station, 5984 Matredal, Norway"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8994-0052","authenticated-orcid":false,"given":"Tina","family":"Oldham","sequence":"additional","affiliation":[{"name":"Institute of Marine Research, Matre Research Station, 5984 Matredal, Norway"}]}],"member":"1968","published-online":{"date-parts":[[2023,9,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1111\/jfd.13167","article-title":"Where art thou louse? A snapshot of attachment location preferences in salmon lice on Atlantic salmon hosts in sea cages","volume":"43","author":"Bui","year":"2020","journal-title":"J. Fish Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1111\/jfd.12061","article-title":"Salmon lice\u2014Impact on wild salmonids and salmon aquaculture","volume":"36","author":"Torrissen","year":"2013","journal-title":"J. Fish Dis."},{"key":"ref_3","first-page":"185","article-title":"Aspects of the biology of the parasitic copepods Lepeophtheirus salmonis and Caligus elongatus on farmed salmonids, and their treatment","volume":"81","author":"Wootten","year":"1982","journal-title":"Proc. Royal Soc. Edinb."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"McEwan, G.F., Groner, M.L., Fast, M.D., Gettinby, G., and Revie, C.W. (2015). Using agent-based modelling to predict the role of wild refugia in the evolution of resistance of sea lice to chemotherapeutants. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0139128"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"929","DOI":"10.1139\/z91-138","article-title":"The developmental stages of Lepeophtheirus salmonis (Kr\u00f8yer, 1837) (Copepoda: Caligidae)","volume":"69","author":"Johnson","year":"1991","journal-title":"Can. J. Zool."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1111\/eva.12505","article-title":"A pedigree-based experiment reveals variation in salinity and thermal tolerance in the salmon louse, Lepeophtheirus salmonis","volume":"10","author":"Ljungfeldt","year":"2017","journal-title":"Evol. Appl."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"237","DOI":"10.3354\/aei00402","article-title":"Farmed salmonids drive the abundance, ecology and evolution of parasitic salmon lice in Norway","volume":"13","author":"Dempster","year":"2021","journal-title":"Aquac. Environ. Interact."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"7865","DOI":"10.1002\/ece3.7618","article-title":"The potential for cleaner fish-driven evolution in the salmon louse Lepeophtheirus salmonis: Genetic or environmental control of pigmentation?","volume":"11","author":"Hamre","year":"2021","journal-title":"Ecol. Evol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Jensen, E.M., Horsberg, T.E., Sevatdal, S., and Helgesen, K.O. (2020). Trends in de-lousing of Norwegian farmed salmon from 2000\u20132019\u2014Consumption of medicines, salmon louse resistance and non-medicinal control methods. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0240894"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1806","DOI":"10.1093\/icesjms\/fsaa062","article-title":"Aquaculture-driven evolution: Distribution of pyrethroid resistance in the salmon louse throughout the North Atlantic in the years 2000\u20132017","volume":"77","author":"Nilsen","year":"2020","journal-title":"ICES J. Mar. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Besnier, F., Kent, M., Skern-Mauritzen, R., Lien, S., Malde, K., Edvardsen, R.B., Taylor, S., Ljungfeldt, L.E.R., Nilsen, F., and Glover, K.A. (2014). Human-induced evolution caught in action: SNP-array reveals rapid amphi-atlantic spread of pesticide resistance in the salmon ecotoparasite Lepeophtheirus salmonis. BMC Genom., 15.","DOI":"10.1186\/1471-2164-15-937"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Ljungfeldt, L.E.R., Espedal, P.G., Nilsen, F., Skern-Mauritzen, M., and Glover, K.A. (2014). A common-garden experiment to quantify evolutionary processes in copepods: The case of emamectin benzoate resistance in the parasitic sea louse Lepeophtheirus salmonis. BMC Evol. Biol., 14.","DOI":"10.1186\/1471-2148-14-108"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.aquaculture.2013.12.033","article-title":"The use of lumpfish (Cyclopterus lumpus L.) to control sea lice (Lepeophtheirus salmonis Kr\u00f8yer) infestations in intensively farmed Atlantic salmon (Salmo salar L.)","volume":"424\u2013425","author":"Imsland","year":"2014","journal-title":"Aquaculture"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/s10164-014-0397-1","article-title":"Notes on the behaviour of lumpfish with and without Atlantic salmon present","volume":"32","author":"Imsland","year":"2014","journal-title":"J. Ethol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/j.aquaculture.2014.06.008","article-title":"Assessment of growth and sea lice infection levels in Atlantic salmon stocked in small-scale cages with lumpfish","volume":"433","author":"Imsland","year":"2014","journal-title":"Aquaculture"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Imsland, A.K., Hanssen, A., Reynolds, P., Nytr\u00f8, A.V., Jonassen, T.M., Hangstad, T.A., Elveg\u00e5rd, T.A., Urskog, T.C., and Mikalsen, B. (2018). It works! Lumpfish can significantly lower sea lice infections in large scale salmon farming. Biol. Open, 7.","DOI":"10.1242\/bio.036301"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1398","DOI":"10.1111\/raq.12299","article-title":"Salmon lice treatments and salmon mortality in Norwegian aquaculture: A review","volume":"11","author":"Overton","year":"2019","journal-title":"Rev. Aquac."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Imsland, A.K.D., and Reynolds, P. (2022). In lumpfish we trust? The efficacy of lumpfish to control Lepeophtheirus salmonis infestations on farmed Atlantic salmon: A review. Fishes, 7.","DOI":"10.3390\/fishes7050220"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.aquaculture.2014.10.048","article-title":"Feeding preferences of lumpfish (Cyclopterus lumpus L.) maintained in open net-pens with Atlantic salmon (Salmo salar L.)","volume":"436","author":"Imsland","year":"2015","journal-title":"Aquaculture"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"698","DOI":"10.1111\/faf.12198","article-title":"Cleaner fishes and shrimp diversity and a re-evaluation of cleaning symbioses","volume":"18","author":"Vaughan","year":"2017","journal-title":"Fish Fish."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"31","DOI":"10.3354\/aei00345","article-title":"Sea lice removal by cleaner fish in salmon aquaculture: A review of the evidence base","volume":"12","author":"Overton","year":"2020","journal-title":"Aquac. Environ. Interact."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Thompson, C.R.S., Madaro, A., Nilsson, J., Stien, L.H., Oppedal, F., \u00d8verli, \u00d8., Korzan, W.J., and Bui, S. (2023). Comparison of non-medicinal delousing strategies for parasite (Lepeophtheirus salmonis) removal efficacy and welfare impact on Atlantic salmon (Salmo salar) hosts. Aquac. Int.","DOI":"10.1007\/s10499-023-01167-8"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1992","DOI":"10.1111\/jiec.13118","article-title":"Quantifying environmental impacts of cleaner fish used as sea lice treatments in salmon aquaculture with life cycle assessment","volume":"26","author":"Philis","year":"2022","journal-title":"J. Ind. Ecol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/j.aquaculture.2014.07.028","article-title":"The effect of temperature and fish size on growth of juvenile lumpfish (Cyclopterus lumpus L.)","volume":"434","author":"Vikingstad","year":"2014","journal-title":"Aquaculture"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1136\/vr.104966","article-title":"Sustainable production and use of cleaner fish for the biological control of sea lice: Recent advances and current challenges","volume":"183","author":"Brooker","year":"2018","journal-title":"Vet. Rec."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/0165-7836(93)90136-U","article-title":"Observations on the distribution of lumpsucker (Cyclopterus lumpus, L.) in the Norwegian Sea","volume":"17","author":"Holst","year":"1993","journal-title":"Fish. Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1016\/j.aquaculture.2016.03.047","article-title":"Is cleaning behavior in lumpfish (Cycloptherus lumpus) parentally controlled?","volume":"459","author":"Imsland","year":"2016","journal-title":"Aquaculture"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1932","DOI":"10.1890\/06-2038.1","article-title":"Escape from UV threats in zooplankton: A cocktail of behavior and protective pigmentation","volume":"88","author":"Hansson","year":"2007","journal-title":"Ecology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1574-6968.2007.00650.x","article-title":"Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites?","volume":"269","author":"Oren","year":"2007","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"4260","DOI":"10.1073\/pnas.0912748107","article-title":"Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators","volume":"107","author":"Scoville","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.aquaculture.2018.11.026","article-title":"Effects of different feeding frequencies on growth, cataract development and histopathology of lumpfish (Cyclopterus lumpus L.)","volume":"501","author":"Imsland","year":"2019","journal-title":"Aquaculture"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1007\/s10499-014-9840-0","article-title":"Assessment of suitable substrates for lumpfish in sea pens","volume":"23","author":"Imsland","year":"2015","journal-title":"Aquac. Int."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"102015","DOI":"10.1016\/j.aquaeng.2019.102015","article-title":"Money for nothing: The possible use of recycled fish farm material as habitat for lumpfish","volume":"87","author":"Imsland","year":"2019","journal-title":"Aquac. Eng."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1469","DOI":"10.1007\/s10499-018-0298-3","article-title":"Assessment of artificial substrates for lumpfish: Effect of material thickness and water current speed","volume":"26","author":"Imsland","year":"2018","journal-title":"Aquac. Int."},{"key":"ref_35","unstructured":"R Core Team (2022, April 10). R: A Language and Environment for Statistical Computing. (v4.1.2). Available online: https:\/\/www.r-project.org\/."},{"key":"ref_36","unstructured":"Fox, J., and Weisberg, S. (2019). An R Companion to Applied Regression, Sage. [3rd ed.]. Available online: https:\/\/socialsciences.mcmaster.ca\/jfox\/Books\/Companion\/."},{"key":"ref_37","unstructured":"Zar, J.H. (1984). Biostatistical Analysis, Prentice-Hall, Inc.. [2nd ed.]."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"737066","DOI":"10.1016\/j.aquaculture.2021.737066","article-title":"Behavioural and physiological responses of lumpfish (Cyclopterus lumpus) exposed to Atlantic salmon (Salmo salar) sensory cues","volume":"544","author":"Staven","year":"2021","journal-title":"Aquaculture"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1214","DOI":"10.1093\/icesjms\/fsy015","article-title":"Production, mortality, and infectivity of planktonic larval sea lice, Lepeophtheirus salmonis (Kr\u00f8yer, 1837): Current knowledge and implications for epidemiological modelling","volume":"75","author":"Brooker","year":"2018","journal-title":"ICES J. Mar. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"836","DOI":"10.1111\/raq.12501","article-title":"Fish welfare in offshore salmon aquaculture","volume":"13","author":"Hvas","year":"2021","journal-title":"Rev. Aquac."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"843","DOI":"10.1016\/j.ijpara.2019.06.003","article-title":"Snorkel sea-cage technology decreases salmon louse infestation by 75% in a full-cycle commercial test","volume":"49","author":"Geitung","year":"2019","journal-title":"Int. J. Parasitol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"735623","DOI":"10.1016\/j.aquaculture.2020.735623","article-title":"Cleaner fish growth, welfare and survival in Atlantic salmon sea cages during an autumn-winter production","volume":"528","author":"Geitung","year":"2020","journal-title":"Aquaculture"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.aquaculture.2018.05.024","article-title":"Application of passive-acoustic telemetry to explore the behaviour of ballan wrasse (Labrus bergylta) and lumpfish (Cyclopterus lumpus) in commercial Scottish salmon sea-pens","volume":"495","author":"Leclercq","year":"2018","journal-title":"Aquaculture"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"67","DOI":"10.3354\/aei00348","article-title":"Sea lice prevention strategies affect cleaner fish delousing efficacy in commercial Atlantic salmon sea cages","volume":"12","author":"Gentry","year":"2020","journal-title":"Aquac. Environ. Interact."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"429","DOI":"10.3354\/aei00320","article-title":"Development of the salmon louse Lepeophtheirus salmonis parasitic stages in temperatures ranging from 3 to 24 \u00b0C","volume":"11","author":"Hamre","year":"2019","journal-title":"Aquac. Environ. Interact."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1841","DOI":"10.1139\/cjfas-2016-0050","article-title":"Salmon lice (Lepeophtheirus salmonis) development times, body size, and reproductive outputs follow universal models of temperature dependence","volume":"73","author":"Samsing","year":"2016","journal-title":"Can. J. Fish. Aquat. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.1111\/raq.12528","article-title":"Evolution of salmon lice in response to management strategies: A review","volume":"13","author":"Coates","year":"2021","journal-title":"Rev. Aquac."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.aquaculture.2008.06.042","article-title":"The effect of temperature and fish size on growth, feed intake, food conversion efficiency and stomach evacuation rate of Atlantic salmon post-smolts","volume":"283","author":"Handeland","year":"2008","journal-title":"Aquaculture"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1570","DOI":"10.1111\/j.1095-8649.2001.tb02313.x","article-title":"Artificial light and season affects vertical distribution and swimming behaviour of post-smolt Atlantic salmon in sea cages","volume":"58","author":"Oppedal","year":"2001","journal-title":"J. Fish Biol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/j.parint.2009.08.009","article-title":"Establishment and characterisation of salmon louse (Lepeophtheirus salmonis (Kr\u00f8yer 1837)) laboratory strains","volume":"58","author":"Hamre","year":"2009","journal-title":"Paras Int."}],"container-title":["Fishes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2410-3888\/8\/9\/455\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:48:18Z","timestamp":1760129298000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2410-3888\/8\/9\/455"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,10]]},"references-count":50,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2023,9]]}},"alternative-id":["fishes8090455"],"URL":"https:\/\/doi.org\/10.3390\/fishes8090455","relation":{},"ISSN":["2410-3888"],"issn-type":[{"value":"2410-3888","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,9,10]]}}}