Marine Biology

, Volume 160, Issue 10, pp 2591–2596 | Cite as

Sub-lethal exposure to ultraviolet radiation reduces prey consumption by Atlantic cod larvae (Gadus morhua)

  • Yuichi FukunishiEmail author
  • Howard I. Browman
  • Caroline M. F. Durif
  • Reidun M. Bjelland
  • Steven D. Shema
  • David M. Fields
  • Anne Berit Skiftesvik
Original Paper


Levels of ultraviolet-B radiation (UV-B: 280–315 nm) reaching the earth’s surface have increased over the past few decades due to ozone depletion. It is well documented that exposure to UV-B radiation increases mortality in marine fish larvae. However, few studies have examined sub-lethal effects of UV-B radiation such as, for example, the possibility that it affects prey consumption by fish larvae. Atlantic cod larvae were exposed to a sub-lethal level of ultraviolet-B radiation (UV-B: 280–315 nm) for 15 h. After the exposure, rotifers (4/mL) were fed to cod larvae at three different post-exposure intervals (20 min, 3 and 6 h). Trials were replicated three times for each post-exposure interval. The number of rotifers in the gut and the percent of empty guts (number of fish with empty gut/number of fish examined × 100) were analyzed. Results were compared to those of unexposed fish (the control treatment). UV-B exposed cod larvae had consumed significantly fewer rotifers than control fish at all post-exposure intervals. There was no significant difference in the frequency of empty guts between fish in the UV-B treatment versus fish in the control treatment at any of the post-exposure time points (although the difference at 20 min post-exposure was borderline significant). These observations suggest that cod larvae exposed to sub-lethal levels of UV-B have lower net energy gain which may lead to reduced growth rate and possibly poorer survival.


Fish Larva Prey Consumption Indian Major Carp Exposure Tank Reduce Prey Consumption 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are grateful for the technical support provided by the staff of the Institute of Marine Research’s Austevoll Research Station. YF was supported by the FY 2010 Researcher Exchange Program between the Japan Society for the Promotion of Science and the Research Council of Norway; Project number: 201981. This research was supported by the Norwegian Institute of Marine Research (Fine-scale interactions in the plankton-Project 11529—to HIB) and the Research Council of Norway project “Cascading effects of climate change and UV envirotoxins on the nutritional quality of the food base in marine ecosystems (Project # 178731/S40 to HIB).


  1. Alemanni ME, Lozada M, Zagarese HE (2003) Assessing sublethal effects of ultraviolet radiation in juvenile rainbow trout (Oncorhynchus mykiss). Photochem Photobiol Sci 2:867–870. doi: 10.1039/b301564e CrossRefGoogle Scholar
  2. Béland F, Browman HI, Rodriguez CA, St-Pierre JF (1999) Effect of solar ultraviolet radiation (280–400 nm) on the eggs and larvae of Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 56:1058–1067Google Scholar
  3. Browman HI, Rodriguez CA, Bèland F, Cullen JJ, Davis RF et al (2000) Impact of ultraviolet radiation on marine crustacean zooplankton and ichthyoplankton: a synthesis of results from the estuary and Gulf of St. Lawrence, Canada. Mar Ecol Prog Ser 199:293–311. doi: 10.3354/meps199293 CrossRefGoogle Scholar
  4. Browman HI, Vetter RD, Rodriguez CA, Cullen JJ, Davis RF et al (2003) Ultraviolet (280–400 nm)-induced DNA damage in the eggs and larvae of Calanus finmarchicus G. (Copepoda) and Atlantic cod (Gadus morhua). Photochem Photobiol 77:397–404. doi: 10.1562/0031-8655(2003)0770397UNDDIT2.0.CO2 CrossRefGoogle Scholar
  5. Dong Q, Svoboda K, Tiersch TR, Monroe WT (2007) Photobiological effects of UVA and UVB light in zebrafish embryos: evidence for a competent photorepair system. J Photochem Photobiol B 88:137–146. doi: 10.1016/j.jphotobiol.2008.07.011 CrossRefGoogle Scholar
  6. Dower JF, Pepin P, Leggett WC (2002) Using patch studies to link mesoscale patterns of feeding and growth in larval fish to environmental varaiability. Fish Oceanogr 11:219–232. doi: 10.1046/j.1365-2419.2002.00197.x CrossRefGoogle Scholar
  7. Ellertsen B, Solemdal P, Strøme T, Tilseth S, Westgåd T et al (1980) Some biological aspects of cod larvae (Gadus morhua L.). Fiskeridirektoratets Skrifter. Serie Havundersøekelser 17:29–47Google Scholar
  8. Fukunishi Y, Masuda R, Yamashita Y (2006) Ontogeny of tolerance to and avoidance of ultraviolet radiation in red sea bream Pagrus major and black sea bream Acanthopagrus schlegeli. Fish Sci 72:356–363. doi: 10.111/j.1444-2906.2006.01157.x CrossRefGoogle Scholar
  9. Fukunishi Y, Browman HI, Durif CMF, Bjelland RM, Skiftesvik AB (2012) Effect of sub-lethal exposure to ultraviolet radiation on the escape performance of Atlantic cod larvae (Gadus morhua). PLoS One 7:e35554. doi: 10.1371/journal.pone.0035554 CrossRefGoogle Scholar
  10. Häder 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 CrossRefGoogle Scholar
  11. Houde ED (1978) Critical food concentrations for larvae of three species of subtropical marine fishes. Bull Mar Sci 28:395–411Google Scholar
  12. Houde ED (1987) Fish early life dynamics and recruitment variability. Am Fish Soc Symp 2:17–29Google Scholar
  13. Hunter JR, Taylor JH, Moser HG (1979) Effect of ultraviolet irradiation on eggs and larvae of the northern anchovy, Engraulis mordax, and the pacific mackerel, Scomber japonicus, during the embryonic stage. Photochem Photobiol 29:325–338. doi: 10.1111/j.1751-1097.1979.tb07055.x CrossRefGoogle Scholar
  14. Hunter JR, Kaupp SE, Taylor JH (1981) Effects of solar and artificial ultraviolet-B radiation on larval northern anchovy, Engraulis mordax. Photochem Photobiol 34:477–486. doi: 10.1111/j.1751-1097.1981.tb09028.x Google Scholar
  15. Huwer B, Clemmesen C, Gronkjaer P, Koster FW (2011) Vertical distribution and growth performance of Baltic cod larvae—field evidence for starvation-induced recruitment regulation during the larval stage? Prog Oceanogr 91:382–396. doi: 10.1016/j.pocean.2011.04.001 CrossRefGoogle Scholar
  16. Jokinen IE, Markkula ES, Salo HM, Kuhn P, Nikoskelainen S et al (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 CrossRefGoogle Scholar
  17. Karjalainen J, Viljanen M (1992) Experimental estimation of the food intake of larval vendace (Coregonus albula L.) under field conditions. Hydrobiologia 243/244:203–209CrossRefGoogle Scholar
  18. Kerr JB, McElroy CT (1993) Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion. Science 262:1032–1034CrossRefGoogle Scholar
  19. Kjeldstad B, Frette Ø, Erga SR, Browman HI, Kuhn P et al (2003) UV (280 to 400 nm) optical properties in a Norwegian fjord system and an intercomparison of underwater radiometers. Mar Ecol Prog Ser 256:1–11. doi: 10.3354/meps256001 CrossRefGoogle Scholar
  20. Köster FW, Hinrichsen HH, Schnack D, St John MA, Mackenzie BR et al (2003) Recruitment of Baltic cod and sprat stocks: identification of critical life stages and incorporation of environmental variability into stock-recruitment relationships. Scientia Marina 67:129–154. doi: 10.3989/scimar.2003.67s1129 Google Scholar
  21. Kouwenberg JHM, Browman HI, Cullen JJ, Davis RF, St-Pierre JF et al (1999) Biological weighting of ultraviolet (280–400 nm) induced mortality in marine zooplankton and fish. I. Atlantic cod (Gadus morhua) eggs. Mar Biol 134:269–284. doi: 10.1007/s002270050545 CrossRefGoogle Scholar
  22. Kuhn PS, Browman HI, Davis RF, Cullen JJ, McArthur BL (2000) Modeling the effects of ultraviolet radiation on embryos of Calanus finmarchicus and Atlantic cod (Gadus morhua) in a mixing environment. Limnol Oceanogr 45:1797–1806CrossRefGoogle Scholar
  23. Llabrés M, Agustí S, Fernández M, Canepa A, Maurin F, Vidal F, Duarte CM (2013) Impact of elevated UVB radiation on marine biota: a meta-analysis. Global Ecol Biogeogr 22:131–144. doi: 10.1111/j.1466-8238.2012.00784.x CrossRefGoogle Scholar
  24. Lough RG, Mountain DG (1996) Effect of small-scale turbulence on feeding rates of larval cod and haddock in stratified water on Georges-Bank. Deep Sea ResII 43:1745–1772. doi: 10.1016/S0967-0645(96)00049-5 CrossRefGoogle Scholar
  25. Madronich S, McKenzie RL, Caldwell MM (1995) Changes in ultraviolet radiation reaching the earth’s surface. Ambio 24:143–152Google Scholar
  26. Malloy KD, Holman MA, Mitchell D, Detrich HW (1997) Solar UVB-induced DNA damage and photoenzymatic DNA repair in Antarctic zooplankton. Proc Natl Acad Sci 94:1258–1263. doi: 10.1073/pnas.94.4.1258 CrossRefGoogle Scholar
  27. McFadzen I, Baynes S, Hallam J, Beesley A, Lowe D (2000) Histopathology of the skin of UV-B irradiated sole (Solea solea) and turbot (Scophthalmus maximus) larvae. Mar Environ Res 50:273–277. doi: 10.1016/S0141-1136(00)00085-4 CrossRefGoogle Scholar
  28. McKenzie RL, Aucamp PJ, Bais AF, Bjön LO, Ilyas M (2007) Changes in biologically-active ultraviolet radiation reaching the Earth’s surface. Photochem Photobiol Sci 6:218–231. doi: 10.1016/S1011-1344(98)00182-1 CrossRefGoogle Scholar
  29. Munk P (1995) Foraging behavior of larval cod (Gadus morhua) influenced by prey density and hunger. Mar Biol 122:205–212. doi: 10.1007/BF00348933 Google Scholar
  30. Olson MH, Mitchell DL (2006) Interspecific variation in UV defense mechanisms among temperate freshwater fishes. Photochem Photobiol 82:606–610. doi: 10.1562/2005-08-23-RA-656 CrossRefGoogle Scholar
  31. Pepin P, Dower JF, Davidson FJM (2003) A spatially explicit study of prey-predator interactions in larval fish: assessing the influence of food and predator abundance on larval growth and survival. Fish Oceanogr 12:19–33. doi: 10.1046/j.1365-2419.2003.00221.x CrossRefGoogle Scholar
  32. Rice JA, Crowder LB, Binkowski FP (1987) Evaluating potential sources of mortality for larval bloater (Coregonus hoyi): starvation and vulnerability to predation. Can J Fish Aqua Sci 44:467–472. doi: 10.1139/f87-055 CrossRefGoogle Scholar
  33. Ruzicka JJ, Gallager SM (2006) The saltatory search behavior of larval cod (Gadus morhua). Deep Sea ResII 53:2735–2757. doi: 10.1016/jdsr2.2006.09.003 CrossRefGoogle Scholar
  34. Sharma J, Rao YV, Kumar S, Chakrabarti R (2010) Impact of UV-B radiation on the digestive enzymes and immune system of larvae of Indian major carp Catla catla. Int J Radiat Biol 86:181–186. doi: 10.3109/09553000903419312 CrossRefGoogle Scholar
  35. Sutela T, Huusko A (1994) Digestion of zooplankton in the alimentary tract of vendace (Coregonus albula) larvae. J Fish Biol 44:591–596CrossRefGoogle Scholar
  36. Tedetti M, Sempèrè R (2006) Penetration of ultraviolet radiation in the marine environment. A review. Photochem Photobiol 82:389–397. doi: 10.1562/2005-11-09-IR-733 CrossRefGoogle Scholar
  37. Tilseth S, Ellertsen B (1984) Food consumption rate and gut evacuation processes of first feeding cod larvae (Gadus morhua L.). In: Dahl E, Danielssen DS, Moksness E, Solemdal P (eds) The propagation of cod Gadus morhua L., Flødevigen rapportser vol 1, pp 167–182Google Scholar
  38. Tucker AJ, Williamson CE (2011) Lakes in a new light: indirect effects of ultraviolet radiation. Freshw Rev 4:115–134. doi: 10.1608/FRJ-4.2.472 Google Scholar
  39. Vehniänen ER, Häkinen JM, Oikari AOJ (2007) Responses to ultraviolet radiation in larval pike, Esox lucius, of two origins and ages. Boreal Environ Res 12:673–680Google Scholar
  40. Vetter RD, Kurtzman A, Mori T (1999) Diel cycles of DNA damage and repair in eggs and larvae of northern anchovy, Engraulis mordax, exposed to solar ultraviolet radiation. Photochem Photobiol 69:27–33. doi: 10.1111/j.1751-1097.1999.tb05302.x CrossRefGoogle Scholar
  41. Ylöen I, Heikkila J, Karjalainen J (2004) Metabolic depression in UV-B exposed larval coregonids. Ann Zool Fenn 41:577–585Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Yuichi Fukunishi
    • 1
    Email author
  • Howard I. Browman
    • 2
  • Caroline M. F. Durif
    • 2
  • Reidun M. Bjelland
    • 2
  • Steven D. Shema
    • 3
  • David M. Fields
    • 3
  • Anne Berit Skiftesvik
    • 2
  1. 1.Maizuru Fisheries Research StationKyoto UniversityKyotoJapan
  2. 2.Austevoll Research StationInstitute of Marine ResearchStorebøNorway
  3. 3.Bigelow Laboratory for Ocean SciencesEast BoothbayUSA

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