Long-Term Effect of Photoperiod, Temperature and Feeding Regimes on the Respiration Rates of Antarctic Krill (Euphausia superba)


Antarctic krill is thought to undergo an annual cycle of biological processes to cope with seasonal changes in their environment. The question of whether, and to what degree, seasonal environmental parameters such as photoperiod, food availability and temperature govern metabolism in krill is not clear. In this long-term laboratory study, respiration rates were determined in krill incubated under simulated natural light cycle or total darkness, subjected to fed or starved conditions and on krill kept at different temperatures (-1°C, 1°C and 3°C). There was a strong and significant increasing trend of respiration rates with month in all experimental treatments. In August (late winter), the mean respiration rates ranged between 0.22 - 0.35 μL O2 mg.DW-1.hr-1 for krill in both simulated seasonal light and complete darkness, and 0.25 - 0.26 μL O2 mg.DW-1.hr-1 for both fed and starved krill. Mean maximal respiration rates were recorded in October and December for all light and feeding treatments (0.46 - 0.56 μL O2 mg.DW-1.hr-1). Mean respiration rates for krill in the temperature treatments ranged between 0.24 - 0.30 μL O2 mg.DW-1.hr-1 in September reaching mean maximal rates in November and February (0.60 - 0.71 μL O2 mg.DW-1.hr-1). The covariate total length of krill was found to be non-significant and there was generally no significant interaction of experimental treatment with month and only for photoperiod comparison was the treatment main effect significant. The dark treatment gave higher respiration rates, and this needs careful interpretation. Results here suggest that, although light, food availability and temperature significantly affect metabolic rates, overal

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M. Brown, S. Kawaguchi, S. Candy, T. Yoshida, P. Virtue and S. Nicol, "Long-Term Effect of Photoperiod, Temperature and Feeding Regimes on the Respiration Rates of Antarctic Krill (Euphausia superba)," Open Journal of Marine Science, Vol. 3 No. 2A, 2013, pp. 40-51. doi: 10.4236/ojms.2013.32A005.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] I. Everson, “Krill Biology, Ecology and Fisheries,” Blackwell Science, Oxford, 2000.
[2] D. G. M. Miller and I. Hampton, “Biology and Ecology of the Antarctic Krill (Euphausia superba Dana): A Re view,” BIOMASS Scientific Series, Vol. 9, 1989, pp. 1166.
[3] M. Mangel and S. Nicol, “Krill and the Unity of Biol ogy,” Canadian Journal of Fisheries and Aquatic Science, Vol. 57, Suppl. 3, 2000, pp. 15.
[4] S. H. Alonzo, P. V. Switzer and M. Mangel, “An Ecosys temBased Approach to Management: Using Individual Behavior to Predict the Indirect Effects of Antarctic Krill Fisheries on Penguin Foraging,” Journal of Applied Eco logy, Vol. 40, No. 4, 2003, pp. 692702. doi:10.1046/j.13652664.2003.00830.x
[5] L. B. Quetin and R. M. Ross, “Behavioral and Physio logical Characteristics of the Antarctic Krill, Euphausia superba,” American Zoologist, Vol. 31, No. 1, 1991, pp. 4963.
[6] P. Virtue, S. Nicol and P. D. Nichols, “Changes in the Digestive Gland of Euphausia superba during Short Term Starvation: Lipid Class, Fatty Acid and Sterol Con tent and Composition,” Marine Biology, Vol. 117, No. 3, 1993, pp. 441448.
[7] W. Hagen, G. Kattner, A. Terbruggen and E. S. Van Vleet, “Lipid Metabolism of the Antarctic krill Euphausia superba and Its Ecological Implications,” Marine Biology, Vol. 139, No. 1, 2001, pp. 95104. doi:10.1007/s002270000527
[8] W. Hagen, T. Yoshida, P. Virtue, S. Kawaguchi, K. M. Swadling, S. Nicol and P. D. Nichols, “Effect of a Car nivorous Diet on the Lipids, Fatty Acids and Condition of Antarctic Krill, Euphausia superba,” Antarctic Science, Vo. 19, 2007, 183188. doi:10.1017/S0954102007000259
[9] T. Ikeda, and P. Dixon, “Body Shrinkage as a Possible Overwintering Mechanism of the Antarctic Krill (Eu phausia superba Dana),” Journal of Experimental Marine Biology and Ecology, Vol. 62, No. 2, 1982, pp. 143151. doi:10.1016/00220981(82)900880
[10] S. Nicol, M. Stolp, T. G. Cochran, P. Geijsel and J. Mar shall, “Growth and Shrinkage of Antarctic krill Euphau sia superba from the Indian Ocean Sector of the Southern Ocean during Summer,” Marine Ecology Progress Series, Vol. 89, 1992, pp. 175181. doi:10.3354/meps089175
[11] A. Clarke, “Lipid content and composition of Antarctic krill, Euphausia superba Dana,” Journal of Crustacean Biology, Vol. 4, No. 1, 1984, pp. 285294.
[12] W. Hagen, E. S. Van Vleet and G. Kattner, “Seasonal Lipid Storage as Overwintering Strategy of Antarctic Krill,” Marine Ecology Progress Series, Vol. 134, 1996, pp. 8589. doi:10.3354/meps134085
[13] P. Virtue, P. D. Nichols, S. Nicol and G. W. Hosie, “Re productive Tradeoff in Male Antarctic Krill, Euphausia superb,” Marine Biology, Vol. 126, No. 3, 1996, pp. 521527. doi:10.1007/BF00354634
[14] A. Clarke, “The Biochemical Composition of Krill, Euphau sia superba Dana from South Georgia,” Journal of Ex perimental Marine Biology and Ecology, Vol. 43, No. 3, 1980, pp. 221236. doi:10.1016/00220981(80)900490
[15] J. Mauchline, “The Biology of Mysids and Euphausiids (Advanced Marine Biology, 18),” Academic Press, Waltham, 1980, pp. 1677.
[16] H. J. Price, K. R. Boyd and C. M. Boyd, “Omnivorous Feeding Behavior of the Antarctic Krill Euphausia superb,” Marine Biology. Vol. 97, No. 1, 1988, pp. 6777. doi:10.1007/BF00391246
[17] M. E. Huntley, W. Nordhausen and M. D. G. Lopez, “Elemental Composition, Metabolic Activity and Growth of Antarctic Krill Euphausia superba during Winter,” Marine Ecology Progress Series, Vol. 107, 1994, pp. 2340. doi:10.3354/meps107023
[18] A. Atkinson, B. Meyer, D. Stübing, W. Hagen, K. Schmidt and U. V. Bathmann, “Feeding and Energy Budgets of Antarctic Krill Euphausia superba at the Onset of Winter II. Juveniles and Adults,” Limnology and Oceanography, Vol. 47, No. 4, 2002, 953966. doi:10.4319/lo.2002.47.4.0953
[19] H. P. Marschall, “The Overwintering Strategy of Antarc tic Krill under the Pack Ice of the Weddell Sea,” Polar Biology, Vol. 9, No. 2, 1988, pp. 129135. doi:10.1007/BF00442041
[20] J. J. Stretch, P. P. Hamner, W. M. Hamner, W. C. Michel, J. Cook and C. W. Sullivan, “Foraging Behavior of Ant arctic Krill Euphausia superba on Sea Ice Microalgae,” Marine Ecology Progress Series, Vo. 44, No. 2, 1988, pp. 131139. doi:10.3354/meps044131
[21] K. Kawaguchi, S. Ishikawa and T. Matsuda, “The Overwintering Strategy of Antarctic Krill (Euphausia superba Dana) under the Coastal Fast Ice off the Ongul Islands in LützolHolm Bay, Antarctica,” Memoirs of the National Institute of Polar Research, Vol. 44, 1986, pp. 6785.
[22] J. J. Torres, J. Donnelly, T. L. Hopkins, T. M. Lancraft, A. V. Aarset and D. G. Ainley, “Proximate Composition and Overwintering Strategies of Antarctic Micronektonic Cru stacea,” Marine Ecology Progress Series, Vol. 113, No. 3, 1994, pp. 221232. doi:10.3354/meps113221
[23] S. RakusaSuszczewski and K. W. Opalinski, “Oxygen Consumption in Euphausia superba,” Polskie Archiwum Hydrobiologii, Vol. 25, No. 3, 1978, pp. 633641.
[24] S. Segawa, M. Kato and M. Murano, “Oxygen Consump tion of the Antarctic Krill,” Transactions of the Tokyo University of Fisheries, Vol. 3, 1979, pp. 113119.
[25] S. Segawa, M. Kato and M. Murano, “Respiration and Ammonia Excretion Rates of the Antarctic Krill, Eu phausia superba Dana,” Transactions of the Tokyo Uni versity of Fisheries, Vol. 5, 1982, pp. 177187.
[26] T. Ikeda and A. W. Mitchell, “Oxygen Uptake, Ammonia Excretion and Phosphate Excretion by Krill and Other Antarctic Zooplankton in Relation to Their Body Size and Chemical Composition,” Marine Biology, Vol. 71, No. 3, 1982, pp. 283298. doi:10.1007/BF00397045
[27] H. J. Hirche, “Excretion and Respiration of the Antarctic Krill Euphausia superba,” Polar Biology, Vol. 1, No. 4, 1983, pp. 205209. doi:10.1007/BF00443189
[28] T. Ikeda, “Sequence in Metabolic Rates and Elemental Composition (C, N, P) during the Developmental of Eu phausia superba Dana and Estimated Food Require ments during Its Life Span,” Journal of Crustacean Biol ogy, Vol. 4, No. 1, 1984, pp. 273284.
[29] T. Ikeda and P. Dixon, “The Influence of Feeding on the Metabolic Activity of Antarctic Krill (Euphausia superba Dana),” Polar Biology, Vol. 3, No. 1, 1984, pp. 19. doi:10.1007/BF00265561
[30] K. W. Opalinski, “Respiratory metabolism and metabolic adaptations of Antarctic krill Euphausia superb,” Polskie Archiwum Hydrobiologii, Vol. 38, No. 2, 1991, pp. 183263.
[31] K. M. Swadling, D. A. Ritz, S. Nicol, J. E. Osborn and L. J. Gurney, “Respiration Rate and Cost of Swimming for Antarctic Krill, Euphausia superba, in Large Groups in the Laboratory,” Marine Biology, Vol. 146, No. 6, 2005, pp. 11691175. doi:10.1007/s002270041519z
[32] M. Teschke, S. Kawaguchi and B. Meyer, “Simulated Light Regimes Affect Feeding and Metabolism of Antarc tic Krill, Euphausia superb,” Limnology and Oceanog raphy, Vo. 52, No. 3, 2007, pp. 10461054. doi:10.4319/lo.2007.52.3.1046
[33] A. Atkinson and R. Snyder, “KrillCopepod Interactions at South Georgia Antarctica, I. Omnivory by Euphausia superb,” Marine Ecology Progress Series, Vol. 160, 1997, pp. 6376. doi:10.3354/meps160063
[34] Y. Hirano, T. Matsuda and S. Kawaguchi, “Breeding Krill in Captivity,” Marine and Freshwater Behavior and Physiology, Vol. 36, No. 4, 2003, pp. 249258. doi:10.1080/10236240310001623637
[35] M. Brown, S. Kawaguchi, R. King, P. Virtue and S. Nicol, “Flexible Adaptation of the Seasonal Krill Maturity Cycle in the Laboratory,” Journal of Plankton Research, Vol. 33, No. 5, 2011, pp. 821826. doi:10.1093/plankt/fbq123
[36] G. A. Knox, “Biology of the Southern Ocean,” Cam bridge University Press, Cambridge, 1994.
[37] R. G. Hartnoll, “Growth in Crustacea—Twenty Years on,” Hydrobiologia, Vol. 449, No. 13, 2001, pp. 111122. doi:10.1023/A:1017597104367
[38] M. A. McWhinnie and P. Marciniak, “Temperature Re sponses and Tissue Respiration in Antarctic Crustacea with Particular Reference to the Krill Euphausia super ba,” Antarctic Research Series, Vol. 1, 1964, pp. 6372. doi:10.1029/AR001p0063
[39] B. Meyer, “The Overwintering of Antarctic Krill, Euph ausia superba, from an Ecophysiological Perspective,” Polar Biology, Vol. 35, No. 1, 2012, pp. 1537. doi:10.1007/s0030001111200
[40] A. de. C. Baker, M. R. Clarke and M. J. Harris, “The N.I.O. Combination Net (RMT) 1 + 8 and Further De velopments of Rectangular Midwater Trawls,” Journal of Marine Biological Association of the United Kingdom, Vol. 53, No. 1, 1973, pp. 167184. doi:10.1017/S0025315400056708
[41] R. King, S. Nicol, P. Cramp and K. M. Swadling, “Krill Maintenance and Experimentation at the Australian Ant arctic Division,” Marine and Freshwater Behaviour and Physiology, Vol. 36, No. 4, 2003, pp. 271283. doi:10.1080/10236240310001614457
[42] S. Kawaguchi, R. King, R. Meijers, J. E. Osborn, K. M. Swadling, D. A. Ritz and S. Nicol, “An Experimental Aquarium for Observing the Schooling Behaviour of Ant arctic Krill,” Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 57, No. 78, 2010, pp. 683692. doi:10.1016/j.dsr2.2009.10.017
[43] M. Omori and T. Ikeda, “Methods in Marine Zooplankton Ecology,” John Wiley and Sons, New York, 1984.
[44] B. Meyer, A. Atkinson, D. Stübing, B. Oettl, W. Hagen and U. V. Bathmann, “Feeding and Energy Budgets of Antarctic krill Euphausia superba at the Onset of Win ter—I. Furcilia III Larvae,” Limnology and Oceanogra phy, Vo. 47, No. 4, 2002, pp. 943952. doi:10.4319/lo.2002.47.4.0943
[45] D. J. Morris , J. L. Watkins, C. Ricketts, F. Buchholz and J. Priddle, “An Assessment of the Merits of Length and Weight Measurements of Antarctic Krill Euphausia su perba,” British Antarctic Survey Bulletin, Vol. 79, 1988, pp. 2750.
[46] Lawes Agricultural Trust, “GenStat Release 10.2 (PC/ Windows) (Rothamsted, UK),” VSN International Ltd., Hemel Hempstead, 2007.
[47] V. Siegel and V. Loeb, “Recruitment of Antarctic Krill Euphausia superba and Possible Causes for Its Variabil ity,” Marine Ecology Progress Series, Vol. 123, 1995, pp. 4556. doi:10.3354/meps123045
[48] V. Siegel, “Krill (Euphausiacea) Demography and Vari ability in Abundance and Distribution,” Canadian Jour nal of Fisheries and Aquatic Sciences, Vol. 57, Suppl. 3, 2000, pp. 151167.
[49] V. Siegel and S. Nicol, “Population Parameters,” In: I. Everson, Ed., Krill: Biology, Ecology and Fisheries. Blackwell Science, London, 2000, pp. 102149.
[50] A. Clarke and P. A. Tyler, “Adult Antarctic Krill Feeding at Abyssal Depths,” Current Biology, Vol. 18, No. 4, 2008, pp. 282285. doi:10.1016/j.cub.2008.01.059
[51] K. Schmidt, A. Atkinson, S. Steigenberger, S. Fielding, M. C. M. Lindsay, D. W. Pond, G. A. Tarling, T. A. Klevjer, C. S. Allen, S. Nicol and E. P. Achterberg, “Seabed Forag ing by Antarctic Krill: Implications for Stock Assessment, BenthoPelagic Coupling, and the Vertical Transfer of Iron,” Limnology and Oceanography, Vol. 56, No. 4, 2012, pp. 14111428. doi:10.4319/lo.2011.56.4.1411
[52] K. Schmidt, A. Akinson, K. J. Petzke, M. Voss and D. W. Pond, “Protozoans as a Food Source for Antarctic Krill, Euphausia superba: Complementary Insights from Stom ach Content, Fatty Acids, and Stable Isotopes,” Limnol ogy and Oceanography, Vol. 51, No. 5, 2006, pp. 24092427. doi:10.4319/lo.2006.51.5.2409
[53] B. Meyer, L. Auerswald, V. Siegel, S. Spahic, C. Pape, B. A. Fach, M. Teschke, A. L. Lopata and V. Fuentes, “Seasonal Variation in Body Composition, Metabolic Ac tivity, Feeding, and Growth of Adult Krill Euphausia su perba in the Lazarev Sea,” Marine Ecology Progress Se ries, Vol. 398, 2010, pp. 118. doi:10.3354/meps08371
[54] S. Kawaguchi, T. Ichii and M. Naganobu, “Green Krill, the Indicator of Micro and NanoSize Phytoplankton Availability to Krill,” Polar Biology, Vol. 22, No. 2, 1999, pp. 133136. doi:10.1007/s003000050400
[55] S. Nicol, P. Virtue, R. King, S. R. Davenport, A. F. McGaffin and P. D. Nichols, “Condition of Euphausia crystallorophias off East Antarctica in Winter in Com parison to Other Seasons,” Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 51, No. 1719, 2004, pp. 22152224. doi:10.1016/j.dsr2.2004.07.002
[56] C. O’Brien, P. Virtue, S. Kawaguchi and P. D. Nichols, “Aspects of Krill Growth and Condition during Late Win terEarly Spring off East Antarctica (110130°E),” Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 58, No. 910, 2011, pp. 12111221. doi:10.1016/j.dsr2.2010.11.001
[57] J. Wiedenmann, K. Cresswell and M. Mangel, “Temper atureDependent Growth of Antarctic Krill: Predictions for a Changing Climate from a Cohort Model,” Marine Ecology Progress Series, Vol. 358, 2008, pp. 191202. doi:10.3354/meps07350
[58] S. Nicol, “Understanding Krill Growth and Ageing: The Contribution of Experimental Studies,” Canadian Journal of Fisheries and Aquatic Science, Vol. 57, Suppl. 3, 2000, pp. 168177.
[59] M. Brown, S. Kawaguchi, S. Candy and P. Virtue, “Tem perature Effects on the Growth and Maturation of Antarc tic Krill (Euphausia superba),” Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 57, No. 78, 2010, pp. 672682. doi:10.1016/j.dsr2.2009.10.016
[60] A. Atkinson, R. S. Shreeve, A. G. Hirst, P. Rothery, G. A. Tarling, D. Pond, R. E. Korb, E. J. Murphy and J. L. Watkins, “Natural Growth Rates in Antarctic Krill (Euph ausia superba): II. Predictive Models Based on Food, Temperature, Body Length, Sex, and Maturity Stage,” Limnology and Oceanography, Vol. 51, No. 2, 2006, pp. 973987. doi:10.4319/lo.2006.51.2.0973
[61] P. Mayzaud, E. Albessard, P. Virtue and M. Boutoute, “Environmental Constraints on the Lipid Composition and Metabolism of Euphausiids: The Case of Euphausia superba and Meganyctiphanes norvegica,” Canadian Journal of Fisheries and Aquatic Science, Vol. 57, Suppl. 3, 2000, pp. 91103.
[62] N. Iguchi and T. Ikeda, “Effects of Temperature on Meta bolism, Growth and Growth Efficiency of Thysanoessa longipes (Crustacea: Euphausiacea) in the Japan Sea,” Journal of Plankton Research, Vol. 27, No. 1, 2005, pp. 110. doi:10.1093/plankt/fbh146
[63] M. Teschke, S. Wendt, S. Kawaguchi, A. Kramer and B. Meyer, “A Circadian Clock in Antarctic Krill: An Endo genous Timing System Governs Metabolic Output Rhy thms in the Euphausid Species Euphausia superb,” PLoS ONE, Vol. 6, No. 10, 2011, Article ID: e26090. doi:10.1371/journal.pone.0026090
[64] P. G. Thomas and T. Ikeda, “Sexual Regression, Shrink age, ReMaturation and Growth of Spent Female Euphau sia superba in the Laboratory,” Marine Biology, Vol. 95, No. 3, 1987, pp. 357363. doi:10.1007/BF00409565
[65] E. Gaten, G. Tarling, H. Dowse, C. Kyriacou and E. Rosata, “Is Vertical Migration in Antarctic Krill (Euphau sia superba) Influenced by an Underlying Circadian Rhy thm?” Journal of Genetics, Vol. 87, No. 5, 2008, pp. 473483. doi:10.1007/s120410080070y
[66] G. A. Tarling, J. CuzinRoudy and F. Buchholz, “Vertical Migration Behaviour in the Northern Krill Meganycti phanes norvegica Is Influenced by Moult and Reproduc tive Processes,” Marine Ecology Progress Series, Vol. 190, 1999, pp. 253262. doi:10.3354/meps190253
[67] S. Kawaguchi, T. Yoshida, L. Finley, P. Cramp and S. Nicol, “The Krill Maturity Cycle: A Conceptual Model of the Seasonal Cycle in Antarctic Krill,” Polar Biology, Vol. 30, No. 6, 2007, pp. 689698. doi:10.1007/s0030000602262
[68] W. Hagen, “Reproductive Strategies and Energetic Ad aptations of Polar Zooplankton,” Invertebrate Reproduc tion and Development, Vol. 36, No. 13, 1999, pp. 2534. doi:10.1080/07924259.1999.9652674

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