, Volume 47, Issue 12, pp 1181–1192

UVB Radiation Variably Affects n-3 Fatty Acids but Elevated Temperature Reduces n-3 Fatty Acids in Juvenile Atlantic Salmon (Salmo salar)

  • Michael T. Arts
  • Michelle E. Palmer
  • Anne Berit Skiftesvik
  • Ilmari E. Jokinen
  • Howard I. Browman
Original Article


Temperature and ultraviolet B radiation (UVB 290–320 nm) are inextricably linked to global climate change. These two variables may act separately, additively, or synergistically on specific aspects of fish biochemistry. We raised Atlantic Salmon (Salmo salar) parr for 54 days in outdoor tanks held at 12 and 19 °C and, at each temperature, we exposed them to three spectral treatments differing in UV radiation intensity. We quantified individual fatty acid (FA) mass fractions in four tissues (dorsal muscle, dorsal and ventral skin, and ocular tissue) at each temperature × UV combination. FA composition of dorsal muscle and dorsal and ventral skin was not affected by UV exposure. Mass fractions of 16:0, 18:0, and saturated fatty acids (SFA) were greater in dorsal muscle of warm-reared fish whereas 18:3n-3, 20:2, 20:4n-6, 22:5n-3, 22:6n-3, n-3, n-6, polyunsaturated fatty acids (PUFA), and total FA were significantly higher in cold-reared fish. Mass fractions of most of the FA were greater in the dorsal and ventral skin of warm-reared fish. Cold-reared salmon exposed to enhanced UVB had higher ocular tissue mass fractions of 20:2, 20:4n-6, 22:6n-3, n-3, n-6, and PUFA compared to fish in which UV had been removed. These observations forecast a host of ensuing physiological and ecological responses of juvenile Atlantic Salmon to increasing temperatures and UVB levels in native streams and rivers where they mature before smolting and returning to the sea.


Atlantic Salmon Fatty acids Temperature UV radiation Climate change Aquaculture 



Docosahexaenoic acid


Essential fatty acid(s)


Fatty acid(s)


Fatty acid methyl ester(s)


Long-chain polyunsaturated fatty acid(s) (carbon chain length ≥C20 and typically with ≥3 double bonds)


Monounsaturated fatty acid(s)


Polyunsaturated fatty acid(s)


Saturated fatty acid(s)


Ultraviolet A radiation (320–400 nm)


Ultraviolet B radiation (290–320 nm)


Ultraviolet radiation (both UVA and UVB)


  1. 1.
    McKenzie RL, Aucamp PJ, Bais AF, Björn LO, Ilyas M, Madronichg S (2011) Ozone depletion and climate change: impacts on UV radiation. Photochem Photobiol Sci 10:182–198. doi:10.1039/C0PP90034F PubMedCrossRefGoogle Scholar
  2. 2.
    IPCC (2007) Climate Change 2007: The physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M Miller HL (eds) Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press. Cambridge, UK and New York, p 996Google Scholar
  3. 3.
    McKee D, Atkinson D, Collings S, Eaton J, Harvey I, Hatton K, Wilson D, Moss B (2002) Macro-zooplankter responses to simulated climate warming in experimental freshwater microcosms. Freshw Biol 47:1557–1570. doi:10.1046/j.1365-2427.2002.00878.x CrossRefGoogle Scholar
  4. 4.
    Van Doorslaer W, Stoks R, Jeppesen E, De Meester L (2007) Adaptive microevolutionary responses to simulated global warming in Simocephalus vetulus: a mesocosm study. Global Change Biol 13:848–886. doi:10.1111/j.1365-2486.2007.01317.x Google Scholar
  5. 5.
    Rex M, Harris NRP, von der Gathen P, Lehmann R, Braathen GO, Reimer E, Beck A, Chipperfield MP, Alfier R, Allaart M, O’Connor F, Dier H, Dorokhov V, Fast H, Gil M, Kyrö E, Litynska Z, Mikkelsen IS, Molyneux MG, Nakane H, Notholt J, Rummukainen M, Viatte P, Wenger J (1997) Prolonged stratospheric ozone loss in the 1995–96 Arctic winter. Nature 389:835–8388. doi:10.1038/39849 CrossRefGoogle Scholar
  6. 6.
    Sinensky H (1974) Homoviscous adaptation—a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci USA 71:522–525PubMedCrossRefGoogle Scholar
  7. 7.
    Arts MT, Kohler CC (2009) Health and condition in fish: the influence of lipids on membrane competency and immune response. In: Arts MT, Kainz M, Brett MT (eds) Lipids in Aquatic Ecosystems, Springer, New York, pp 237–255. doi: 10.1007/978-0-387-89366-2_10
  8. 8.
    Hader DP, Helbling EW, Williamson CE, Worrest RC (2011) Effects of UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 10:242–260. doi:10.1039/C0PP90036B PubMedCrossRefGoogle Scholar
  9. 9.
    Arts MT, Browman HI, Jokinen I, Skiftesvik AB (2010) Effects of UV radiation and diet on polyunsaturated fatty acids in the skin, ocular tissue and dorsal muscle of Atlantic Salmon (Salmo salar) held in outdoor rearing tanks. Photochem Photobiol 86:909–919. doi:10.1111/j.0031-8655.2010.00733.x PubMedGoogle Scholar
  10. 10.
    Holtby LB, Bothwell ML (2008) Effects of solar ultraviolet radiation on the behaviour of juvenile coho salmon (Oncorhynchus kisutch): avoidance, feeding, and agonistic interactions. Can J Fish Aquat Sci 65:701–711. doi:10.1139/F08-013 CrossRefGoogle Scholar
  11. 11.
    Jokinen IE, Markkula ES, Salo HM, Kuhn P, Nikoskelainen S, Arts MT, Browman HI (2008) Exposure to increased ambient ultraviolet B radiation has negative effects on growth, condition and immune function of juvenile Atlantic Salmon (Salmo salar). Photochem Photobiol 84:1265–1271. doi:10.1111/j.1751-1097.2008.00358.x PubMedCrossRefGoogle Scholar
  12. 12.
    Markkula SE, Karvonen A, Salo H, Valtonen ET, Jokinen EI (2007) Ultraviolet B irradiation affects resistance of rainbow trout (Oncorhynchus mykiss) against bacterium Yersinia ruckeri and trematode Diplostomum spathaceum. Photochem Photobiol 83:1263–1269. doi:10.1111/j.1751-1097.2007.00165.x PubMedCrossRefGoogle Scholar
  13. 13.
    Jokinen IE, Salo HM, Markkula ES, Rikalainen K, Arts MT, Browman HI (2011) Additive effects of enhanced ambient ultraviolet B radiation and increased temperature on immune function, growth and physiological condition of juvenile (parr) Atlantic Salmon, Salmo salar. Fish Shellfish Immun 30:102–108. doi:10.1016/j.fsi.2010.09.017 CrossRefGoogle Scholar
  14. 14.
    Salo HM, Jokinen EI, Markkula SE, Aaltonen TM, Penttilä HT (2000) Comparative effects of UVA and UVB irradiation on the immune system of fish. J Photochem Photobiol B 56:154–162. doi:10.1016/S1011-1344(00)00072-5 PubMedCrossRefGoogle Scholar
  15. 15.
    Kaweewat K, Hofer R (1997) Effect of UV-B radiation on goblet cells in the skin of different fish species. J Photochem Photobiol B Biol 41:222–226. doi:10.1016/S1011-1344(97)00104-8 CrossRefGoogle Scholar
  16. 16.
    Sharma JG, Masuda R, Tanaka M (2005) Ultrastructural study of skin and eye of UV-B irradiated ayu Plecoglossus altivelis. J Fish Biol 67:1646–1652. doi:10.1111/j.1095-8649.2005.00871.x CrossRefGoogle Scholar
  17. 17.
    Bell MV, Batty RS, Dick JR, Fretwell K, Navarro JC, Sargent JR (1995) Dietary deficiency of docosahexaenoic acid impairs vision at low light intensities in juvenile herring (Clupea harengus L.). Lipids 26:565–573. doi:10.1007/BF02536303 CrossRefGoogle Scholar
  18. 18.
    Bell MV, McEvoy LA, Navarro JC (1996) Deficit of didocosahexaenoyl phospholipid in the eyes of larval sea bass fed an essential fatty acid deficient diet. J Fish Biol 49:941–952. doi:10.1111/j.1095-8649.1996.tb00091.x CrossRefGoogle Scholar
  19. 19.
    Jeffrey BG, Weisinger HS, Neuringer M, Mitchell DC (2001) The role of docosahexaenoic acid in retinal function. Lipids 36:859–871. doi:10.1007/s11745-001-0796-3 PubMedCrossRefGoogle Scholar
  20. 20.
    Politi L, Rotstein N, Carri N (2001) Effects of docosahexaenoic acid on retinal development: cellular and molecular aspects. Lipids 36:927–935. doi:10.1007/s11745-001-0803-8 PubMedCrossRefGoogle Scholar
  21. 21.
    Birch EE, Birch DG, Hoffman DR, Uauy R (1992) Dietary essential fatty acid supply and visual acuity development. Invest Ophthalmol Vis Sci 33:3242–3253PubMedGoogle Scholar
  22. 22.
    Rafferty NS, Rafferty KA, Zigman S (1997) Comparative response to UV irradiation of cytoskeletal elements in rabbit and skate lens epithelial cells. Curr Eye Res 16:310–319PubMedCrossRefGoogle Scholar
  23. 23.
    Cullen AP, Monteith-McMaster CA, Sivak JG (1994) Lenticular changes in rainbow trout following chronic exposure to UV-radiation. Curr Eye Res 13:731–737. doi:10.3109/02713689409047007 PubMedCrossRefGoogle Scholar
  24. 24.
    Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509PubMedGoogle Scholar
  25. 25.
    Morrison WR, Smith LM (1964) Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoridemethanol. J Lipid Res 5:600–608PubMedGoogle Scholar
  26. 26.
    Zellmer ID, Arts MT, Abele D, Humbeck K (2004) Evidence of sublethal damage in Daphnia (Cladocera) during exposure to solar UV radiation in subarctic ponds. Arct Antarct Alp Res 36:370–377. doi:10.1657/1523-0430(2004)036[0370:EOSDID]2.0.CO;2 CrossRefGoogle Scholar
  27. 27.
    Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289–300. doi:0035-9246/95/57289 Google Scholar
  28. 28.
    Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River, New Jersey, pp. 210–214. ISBN 10: 013081542X/0-13-081542-XGoogle Scholar
  29. 29.
    Gray JRA, Edington JM (1969) Effect of woodland clearance on stream temperature. J Fish Res Bd Can 26:399–403. doi:10.1139/f69-038 CrossRefGoogle Scholar
  30. 30.
    Brown GW, Krygier JT (1970) Effects of clear-cutting on stream temperature. Water Resour Res 6:1133–1139. doi:10.1029/WR006i004p01133 CrossRefGoogle Scholar
  31. 31.
    Macdonald JS, MacIsaac EA, Herunter HE (2003) The effect of variable-retention riparian buffer zones on water temperatures in small headwater streams in sub-boreal forest ecosystems of British Columbia. Can J For Res 33:1371–1382. doi:10.1139/X03-015 CrossRefGoogle Scholar
  32. 32.
    Schneider P, Hook SJ (2010) Space observations of inland water bodies show rapid surface warming since 1985. Geophys Res Let 37, L22405, p 5. doi:10.1029/2010GL045059
  33. 33.
    Elliott JM, Hurley MA (1997) A functional model for maximum growth of Atlantic salmon parr, Salmo salar, from two populations in northwest England. Funct Ecol 11:592–603. doi:10.1046/j.1365-2435.1997.00130.x CrossRefGoogle Scholar
  34. 34.
    Swansburg E, Chaput G, Moore D, Caissie D, El-Jabi N (2002) Size variability of juvenile Atlantic salmon: links to environmental conditions. J Fish Biol 61:661–683. doi:10.1006/jfbi.2002.2088 CrossRefGoogle Scholar
  35. 35.
    Wagner T, Jones ML, Ebener MP, Arts MT, Brenden TO, Honeyfield DC, Wright GM, Faisal M (2010) Spatial and temporal dynamics of lake whitefish (Coregonus clupeaformis) health indicators: linking individual-based indicators to a management-relevant endpoint 36:121–134. doi: 10.1016/j.jglr.2009.07.004
  36. 36.
    Thonney JP, Gibson RJ (1989) Feeding strategies of brook trout (Salvelinus fontinalis) and juvenile Atlantic salmon (Salmo salar) in a Newfoundland river. Can Field Nat 103:48–56Google Scholar
  37. 37.
    Descroix A, Desvilettes C, Bec A, Martin P, Bourdier G (2010) Impact of macroinvertebrate diet on growth and fatty acid profiles of restocked 0+ Atlantic salmon (Salmo salar) parr from a large European river (the Allier). Can J Fish Aquat Sci 67:659–672. doi:10.1139/F10-012 CrossRefGoogle Scholar
  38. 38.
    Ghioni C, Bell JG, Sargent JR (1996) Polyunsaturated fatty acids in neutral lipids and phospholipids of some freshwater insects. Comp Biochem Physiol B Biochem Mol Biol 114:161–170. doi:10.1016/0305-0491(96)00019-3 CrossRefGoogle Scholar
  39. 39.
    Sushchik NN, Gladyshev MI, Moskvichova AV, Makhutova ON, Kalachova GS (2003) Comparison of fatty acid composition in major lipid classes of the dominant benthic invertebrates of the Yenisei River. Comp Biochem Physiol B 134:111–122. doi:10.1016/S1096-4959(02)00191-4 PubMedCrossRefGoogle Scholar
  40. 40.
    Torres-Ruiz M, Wehr JD, Perrone AA (2007) Trophic relationships in a stream food web: importance of fatty acids for macro-invertebrate consumers. J N Am Benthol Soc 26:509–522. doi:10.1899/06-070.1 CrossRefGoogle Scholar
  41. 41.
    Bell JG, Tocher DR, Farndale BM, Cox DI, McKinney RW, Sargent JR (1997) The effect of dietary lipid on polyunsaturated fatty acid metabolism in Atlantic Salmon (Salmo salar) undergoing parr-smolt transformation. Lipids 32:515–525. doi:10.1007/s11745-997-0066-4 PubMedCrossRefGoogle Scholar
  42. 42.
    Tocher DR, Bell JG, Dick JR, Henderson RJ, McGhee F, Michell D, Morris PC (2000) Polyunsaturated fatty acid metabolism in Atlantic salmon (Salmo salar) undergoing parr-smolt transformation and the effects of dietary linseed and rapeseed oils. Fish Physiol Biochem 23:59–73. doi:10.1023/A:1007807201093 CrossRefGoogle Scholar
  43. 43.
    Sheridan MA, Allen WV, Kerstetter TH (1985) Changes in the fatty acid composition of steelhead trout, Salmo gairdnerii Richardson associated with parr-smolt transformation. Comp Biochem Physiol 80B:671–676. doi:10.1016/0305-0491(85)90444-4 Google Scholar
  44. 44.
    Li H-O, Yamada J (1992) Changes of the fatty acid composition in smolts of masu salmon (Oncorhynchus masou), associated with desmoltification and seawater transfer. Comp Biochem Physiol 103A:221–226. doi:10.1016/0300-9629(92)90266-S CrossRefGoogle Scholar
  45. 45.
    Fuschino JR, Guschina IA, Dobson G, Yan ND, Harwood JL, Arts MT (2011) Rising water temperatures alter lipid dynamics and reduce n-3 essential fatty acid concentrations in Scenedesmus obliquus (Chlorophyta). J Phycol 47:763–774. doi:10.1111/j.1529-8817.2011.01024.x CrossRefGoogle Scholar
  46. 46.
    Gladyshev MI, Sushchik NN, Makhutova ON, Dubovskaya OP, Kravchuk ES, Kalachova GS, Khromechek EB (2010) Correlations between fatty acid composition of seston and zooplankton and effects of environmental parameters in a eutrophic Siberian reservoir. Limnologica 40:343–357. doi:10.1016/j.limno.2009.12.004 CrossRefGoogle Scholar
  47. 47.
    Leibowitz MP, Ariav R, Zilberg D (2005) Environmental and physiological conditions affecting Tetrahymena sp. infection in guppies, Poecilia reticulata Peters. J Fish Dis 28:539–547. doi:10.1111/j.1365-2761.2005.00658.x CrossRefGoogle Scholar
  48. 48.
    Hirazawa N, Takano R, Hagiwara H, Noguchi M, Narita M (2010) The influence of different water temperatures on Neobenedenia girellae (Monogenea) infection, parasite growth, egg production and emerging second generation on amberjack Seriola dumerili (Carangidae) and the histopathological effect of this parasite on fish skin. Aquaculture 299:2–7. doi:10.1016/j.aquaculture.2010.10.029 CrossRefGoogle Scholar
  49. 49.
    Heuch PA, Revie CW, Gettinby G (2003) A comparison of epidemiological patterns of salmon lice, Lepeophtheirus salmonis, infections on farmed Atlantic salmon, Salmo salar L., in Norway and Scotland. J Fish Dis 26:539–551. doi:10.1046/j.1365-2761.2003.00490.x PubMedCrossRefGoogle Scholar
  50. 50.
    Merle C, Laugel C, Baillet-Guffroy A (2010) Effect of UVA or UVB irradiation on cutaneous lipids in films or in solution. Photochem Photobiol 86:553–562. doi:10.1111/j.1751-1097.2009.00690.x PubMedCrossRefGoogle Scholar
  51. 51.
    Bullock AM, Roberts RJ, Waddington P (1983) Sunburn lesions in koi carp. Vet Rec 112:551PubMedCrossRefGoogle Scholar
  52. 52.
    Ramos KT, Fries LT, Berkhouse CS, Fries JN (1994) Apparent sunburn of juvenile paddlefish. Prog Fish Culturist 56:214–216CrossRefGoogle Scholar
  53. 53.
    Blazer VS, Fabacher DL, Little EE, Ewing MS, Kocan KM (1997) Effects of ultraviolet-B radiation on fish: histologic comparison of a UVB-sensitive and a UVB-tolerant species. J Aquat Animal Health 9:132–143CrossRefGoogle Scholar
  54. 54.
    Zamzow JP (2004) Effects of diet, ultraviolet exposure, and gender on the ultraviolet absorbance of fish mucus and ocular structures. Mar Biol 144:1057–1064. doi:10.1007/s00227-003-1286-2 CrossRefGoogle Scholar
  55. 55.
    Treasurer JW, Cox DI, Wall T (2007) Epidemiology of blindness and cataracts in cage reared ongrown Atlantic halibut Hippoglossus hippoglossus. Aquaculture 271:77–84. doi:10.1016/j.aquaculture.2007.05.008 CrossRefGoogle Scholar
  56. 56.
    Bjerkås E, Holst JC, Bjerkås I, Ringvold A (2003) Osmotic cataract causes reduced vision in wild Atlantic salmon postsmolts. Dis Aquat Org 55:151–159. doi:10.3354/dao055151 PubMedCrossRefGoogle Scholar
  57. 57.
    Fliesler SJ, Anderson RE (1983) Chemistry and metabolism of lipids in the vertebrate retina. In: Holman RT (ed) Progress in lipid research, vol 22. Pergamon Press, Oxford, pp 79–131Google Scholar
  58. 58.
    Masuda R, Takeuchi T, Tsukamoto K, Ishizaki Y, Kanematsu M, Imaizumi K (1998) Critical involvement of dietary docosahexaenoic acid in the ontogeny of schooling behaviour in the yellowtail. J Fish Biol 53:471–484. doi:10.1111/j.1095-8649.1998.tb00996.x CrossRefGoogle Scholar
  59. 59.
    Vagner M, Santigosa E (2011) Characterization and modulation of gene expression and enzymatic activity of delta-6 desaturase in teleosts: a review. Aquaculture 315:131–143. doi:10.1016/j.aquaculture.2010.11.031 CrossRefGoogle Scholar
  60. 60.
    Jonsson B, Jonsson N (2009) A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta, with particular reference to water temperature and flow. J Fish Biol 75:2381–2447. doi:10.1111/j.1095-8649.2009.02380.x PubMedCrossRefGoogle Scholar
  61. 61.
    Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260. doi:10.1016/S0169-5347(01)02124-3 PubMedCrossRefGoogle Scholar
  62. 62.
    Blas J, Bortolotti GR, Tella JL, Baos R, Marchant TA (2007) Stress response during development predicts fitness in a wild, long lived vertebrate. Proc Natl Acad Sci USA 104:8880–8884. doi:10.1073/pnas.0700232104 PubMedCrossRefGoogle Scholar
  63. 63.
    Gladyshev M, Arts MT Sushchik NN (2009) Preliminary estimates of the export of omega-3 highly unsaturated fatty acids (EPA + DHA) from aquatic to terrestrial ecosystems. In: Arts MT, Kainz M Brett MT (eds) Lipids in aquatic ecosystems, Springer, NY, pp 179–209. doi: 10.1007/978-0-387-89366-2_8

Copyright information

© Her Majesty the Queen in Right of Canada 2012

Authors and Affiliations

  • Michael T. Arts
    • 1
  • Michelle E. Palmer
    • 2
  • Anne Berit Skiftesvik
    • 3
  • Ilmari E. Jokinen
    • 4
  • Howard I. Browman
    • 3
  1. 1.National Water Research InstituteEnvironment CanadaBurlingtonCanada
  2. 2.Department of BiologyYork UniversityTorontoCanada
  3. 3.Institute of Marine ResearchAustevoll Research StationStorebøNorway
  4. 4.Department of Biological and Environmental ScienceUniversity of JyväskyläJyväskyläFinland

Personalised recommendations