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Physiological response of adult Antarctic krill, Euphausia superba, to long-term starvation

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Abstract

Adult Euphausia superba survive winter without or with little feeding. It is not exactly known whether the scarcity of food or an internal clock, set by the natural Antarctic light regime, are responsible for non-feeding. Our research questions were therefore the following: (1) How will physiological and biochemical conditions of krill change during long-term starvation at constant light regime? (2) If and how do enzyme activities change during such starvation? (3) What is the influence of food availability versus that of light regime? To answer these questions, adult krill were starved under laboratory conditions for 12 weeks with constant light regime (12:12; dark/light) and the impact on physiological functions was studied. Initial experimental condition of krill resembled the condition of late spring krill in the field with fully active metabolism and low lipid reserves. Metabolic activity and activities of enzymes catabolising lipids decreased after the onset of starvation and remained low throughout, whereas lipid reserves declined and lipid composition changed. Mass and size of krill decreased while the inter-moult period increased. Depletion of storage- and structural metabolites occurred in the order of depot lipids and glycogen reserves after onset of starvation until proteins were almost exclusively used after 6–7 weeks of starvation. Results confirmed various proposed overwintering mechanisms such as metabolic slowdown, slow growth or shrinkage and use of lipid reserves. However, these changes were set in motion by food shortage only, i.e. without the trigger of a changing light regime.

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References

  • Atkinson A, Meyer B, Stübing D, Hagen W, Bathmann UV (2002) Feeding and energy budgets of Antarctic krill Euphausia superba at the onset of winter – II. Juveniles and adults. Limnol Oceanogr 47:953–966

    Article  Google Scholar 

  • Auerswald L, Gäde G (1999) The fate of proline in the African fruit beetle Pachnoda sinuata. Insect Biochem Mol Biol 29:687–700

    Article  CAS  Google Scholar 

  • Auerswald L, Gäde G (2000) Metabolic changes in the African fruit beetle, Pachnoda sinuata during starvation. J Insect Physiol 46:343–351

    Article  CAS  PubMed  Google Scholar 

  • Auerswald L, Pape C, Stübing D, Lopata AL, Meyer B (2009) Effect of short-term starvation of adult Antarctic krill, Euphausia superba, at the onset of summer. J Exp Mar Biol Ecol 381:47–56

    Article  Google Scholar 

  • Baker AC, Clarke MR, Harris MJ (1973) The N.I.O. combination net (RMT 1 + 8) and further developments of rectangular midwater trawls. J Mar Biol Assoc UK 53:176–184

    Article  Google Scholar 

  • Beenakkers AMTh, van der Horst DJ, Marrewijk WJA (1984) Insect flight muscle metabolism. Insect Biochem 14:243–260

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of motion-dye-binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brown M, Kawaguchi S, King R, Virtue P, Nicol S (2011) Flexible adaptation of the seasonal krill maturity cycle in the laboratory. J Plankton Res 33:821–826. doi:10.1093/plankt/fbq123

    Article  Google Scholar 

  • Brown M, Kawaguchi S, Candy S, Yoshida T, Virtue P, Nicol S (2013) Long-term effect of photoperiod, temperature and feeding regimes on the respiration rates of Antarctic krill (Euphausia superba) in the laboratory. Open J Mar Sci 3:40–51. doi:10.4236/ojms.2013.32A005

    Article  Google Scholar 

  • Buchholz F (1991) Moult cycle and growth of Antarctic krill Euphausia superba in the laboratory. Mar Ecol Prog Ser 69:217–229

    Article  Google Scholar 

  • Ceccaldi HJ (2006) The digestive tract: Anatomy, physiology, and biochemistry. In: Forest J, von Vaupel Klein JC (eds), The Crustacea II. Leiden: Brill NV, pp 85–203

  • Everson I (ed) (2000) Krill biology, ecology and fisheries. Fish and Aquatic Resources Series 6. Blackwell Science, Oxford. pp 372

  • Falk-Petersen S, Hagen W, Kattner G, Clarke A, Sargent JR (2000) Lipids, trophic relationships and biodiversity in Arctic and Antarctic krill. Can J Fish Aquat Sci 57:178–191

    Article  CAS  Google Scholar 

  • Fraser AJ, Tocher DR, Sargent JR (1985) Thin-layer chromatography flame ionization detection and the quantitation of marine neutral lipids and phospholipids. J Exp Mar Bio Ecol 88:91–99

    Article  CAS  Google Scholar 

  • Hagen W (2000) Lipids. In: Harris RP, Wiebe PH, Lenz J, Skjøldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic Press, London, pp 113–119

    Google Scholar 

  • Hagen W, Van Vleet ES, Kattner G (1996) Seasonal lipid storage as overwintering strategy of Antarctic krill. Mar Ecol Prog Ser 134:85–89

    Article  CAS  Google Scholar 

  • Hagen W, Kattner G, Terbrüggen A, Van Vleet ES (2001) Lipid metabolism of the Antarctic krill Euphausia superba and its ecological implications. Mar Biol 139:95–104

    Article  CAS  Google Scholar 

  • Harding GC, Frazer AJ (1999) Application of the triacylglycerol/sterol condition index to the interpretation of larval lobster Homarus americanus distribution in close proximity to georges bank, Gulf of Maine. Mar Ecol Prog Ser 186:239–254

    Article  CAS  Google Scholar 

  • Ikeda T, Dixon P (1982) Body shrinkage as a possible overwintering mechanism of the Antarctic krill, Euphausia superba dana. J Exp Mar Biol Ecol 62:143–151

    Article  Google Scholar 

  • Ikeda T, Mitchell AW (1982) Oxygen uptake, ammonia excretion and phosphate excretion by krill and other Antarctic zooplankton in relation to their body size and chemical composition. Mar Biol 71:283–298

    Article  Google Scholar 

  • Ikeda T, Torres JJ, Hernández-León S, Geiger SP (2000) Metabolism. In: Harris RP, Wiebe PH, Lenz J, Skjøldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic Press, London, pp 455–520

    Chapter  Google Scholar 

  • Johnson MA, Macaulay MC, Biggs DC (1984) Respiration and excretion within a mass aggregation of Euphausia superba: Implications for krill distribution. J Crust Biol 4:174–184

    Google Scholar 

  • Kattner G, Fricke HSG (1986) Simple gas-liquid chromatography method for the simultaneous determination of fatty acids and alcohols in wax esters of marine organisms. J Chromatogr 361:263–268

    Article  CAS  Google Scholar 

  • Kawaguchi S, Candy SG, Robert King R, Naganobu M, Nicol S (2006) Modelling growth of Antarctic krill. I. Growth trends with sex, length, season, and region. Mar Ecol Prog Ser 306:1–15

  • Kawaguchi S, Nicol S (2007) Learning about Antarctic krill from the fishery. Antarct Sci 19(2):219–230

    Article  Google Scholar 

  • Kawaguchi S, King R, Meijers R, Osborn JE, Swadling KM, Ritz DA, Nicol S (2010) An experimental aquarium for observing the schooling behaviour of Antarctic krill (Euphausia superba). Deep-Sea Res II 57:683–692

    Article  Google Scholar 

  • King R, Nicol S, Cramp P, Swadling KM (2003) Krill maintenance and experimentation at the Australian Antarctic division. Mar Freshw Res Behav Physiol 36:271–283

    Article  Google Scholar 

  • Knotz S, Boersma M, Saborowski R (2006) Microassays for a set of enzymes in individual small marine copepods. Comp Biochem Physiol A 145:406–411

    Article  Google Scholar 

  • Kreibich T, Saborowski R, Hagen W, Niehoff B (2008) Short-term variation of nutritive and metabolic parameters in Temora longicornis females (Crustacea, Copepoda) as a response to diet shift and starvation. Helgol Mar Res 62:241–249

    Article  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Mayzaud P, Conover RJ (1988) O: N atomic ratio as a tool to describe zooplankton metabolism. Mar Ecol Prog Ser 45:289–302

    Article  CAS  Google Scholar 

  • Mazzotta GM, De Pitta C, Benna C, Tosatto SCE, Lanfranchi G, Bertolucci C, Costa R (2010) A cry from the krill. Chronobiol Int 27:425–445

    Article  CAS  PubMed  Google Scholar 

  • Meyer B (2012) The overwintering of Antarctic krill, Euphausia superba, from an ecophysiological perspective. Polar Biol 35:15–37

    Article  Google Scholar 

  • Meyer B, Oettl B (2005) Effects of short-term starvation on composition and metabolism of larval Antarctic krill Euphausia superba. Mar Ecol Prog Ser 292:263–270

    Article  CAS  Google Scholar 

  • Meyer B, Atkinson A, Stübing D, Oettl B, Hagen W, Schmidt K (2002a) Feeding and energy budgets of Antarctic krill Euphausia superba at the onset of winter – I. Furcilia III larvae. Limnol Oceanogr 47:943–952

    Article  Google Scholar 

  • Meyer B, Saborowski R, Atkinson A, Buchholz F, Bathmann U (2002b) Seasonal differences in citrate synthase and digestive enzyme activity in larval and postlarval Antarctic krill, Euphausia superba. Mar Biol 141:855–862

    Article  CAS  Google Scholar 

  • Meyer B, Atkinson A, Blume B, Bathmann UV (2003) Feeding and energy budgets of larval Antarctic krill, Euphausia superba, in summer. Mar Ecol Prog Ser 257:167–178

    Article  Google Scholar 

  • Meyer B, Auerswald L, Siegel V, Spahic S, Pape C, Fach B, Teschke M, Lopata AL, Fuentes V (2010) Seasonal variation in body composition, metabolic activity, feeding and growth of adult krill Euphausia superba in the Lazarev sea. Mar Ecol Prog Ser 398:1–18

    Article  CAS  Google Scholar 

  • New MB (1976) A review of dietary studies with shrimp and prawns. Aquaculture 9:101–144

    Article  CAS  Google Scholar 

  • Nicol S (2000) Understanding krill growth and aging: the contribution of experimental studies. Can J Fish Aquat Sci 57(S3):168–177

    Article  Google Scholar 

  • O’Brien C, Virtue P, Kawaguchi S (2011) Aspects of krill growth and condition during late winter-early spring off East Antarctica (110–130 °E). Deep-Sea Res II 58:1211–1221

    Article  Google Scholar 

  • Parkinson CL (2004) Southern ocean sea ice and its wider linkages: insights revealed from models and observations. Antarct Sci 16:387–400

    Article  Google Scholar 

  • Prim N, Sánchez M, Ruiz C, Pastor FIJ, Diaz P (2003) Use of methylumbeliferyl-derivative substrates for lipase activity characterization. J Mol Catal B: Enzym 22:339–346

    Article  CAS  Google Scholar 

  • Quetin LB, Ross RM, Clarke A (1994) Krill energetics: seasonal and environmental aspects of the physiology of Euphausia superba. In: El-Sayed SZ (ed) Southern ocean ecology: the BIOMASS perspective. Cambridge University Press, Cambridge, pp 165–184

    Google Scholar 

  • Sánchez-Paz A, García-Carreño FL, Muhlia-Almazán A, Peregrino-Uriarte AB, Hernández-López JY, Yepiz-Plascencia G (2006) Usage of energy reserves in crustaceans during starvation: status and future directions. Insect Biochem Mol Biol 36:241–249

    Article  PubMed  Google Scholar 

  • Seear PJ, Geraint AT, Teschke M, Meyer B, Thorne MAS, Clark MS, Gaten E, Rosato E (2009) Effects of simulated light regimes on gene expression in Antarctic krill (Euphausia superba Dana). J Exp Mar Biol Ecol 381:57–64

    Article  CAS  Google Scholar 

  • Seear PJ, Goodall-Copestake WP, Fleming AH, Rosato E, Tarling GA (2012) Seasonal and spatial influences on gene expression in Antarctic krill Euphausia superba. Mar Ecol Prog Ser 467:61–75

    Article  CAS  Google Scholar 

  • Siegel V (2000) Krill (Euphausiacea) life history and aspects of population dynamics. Can J Fish Aquat Sci 57(S3):130–150

    Article  Google Scholar 

  • Siegel V (2012) Krill stocks in high latitudes of the Antarctic Lazarev sea: seasonal and interannual variation in distribution, abundance and demography. Polar Biol 35:1151–1177

    Article  Google Scholar 

  • Siegel V, Loeb V (1995) Recruitment of Antarctic krill Euphausia superba and possible causes for its variability. Mar Ecol Prog Ser 123:45–56

    Article  Google Scholar 

  • Solorzano L (1969) Determination of ammonia in natural waters by the phenol hypochlorite method. Limnol Oceanogr 14:799–801

    Article  CAS  Google Scholar 

  • Stitt M (1984) Citrate synthase (condensing enzyme). In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol IV. Chemie, Weinheim, pp 353–358

    Google Scholar 

  • Stübing D (2004) Lipid biochemistry of Antarctic euphausiids - energetic adaptations and a critical appraisal of trophic markers. Dissertation, University of Bremen

  • Stübing D, Hagen W (2003) Fatty acid biomarker ratios—suitable trophic indicators in Antarctic euphausiids? Polar Biol 26:774–782

    Article  Google Scholar 

  • Stübing D, Hagen W, Schmidt K (2003) On the use of lipid biomarkers in marine food web analyses: an experimental case study on the Antarctic krill, Euphausia superba. Limnol Oceanogr 48:1685–1700

    Article  Google Scholar 

  • Tarling GA, Shreeve RS, Hirst AG, Atkinson A, Pond DW, Murphy EJ, Watkins JL (2006) Natural growth rates in Antarctic krill (Euphausia superba): I. improving methodology and predicting intermolt period. Limnol Oceanogr 51:959–972

    Article  Google Scholar 

  • Teschke M, Kawaguchi S, Meyer B (2007) Simulated light regimes affect feeding and metabolism of Antarctic krill, Euphausia superba. Limnol Oceanogr 52:1046–1054

    Article  Google Scholar 

  • Teschke M, Kawaguchi S, Meyer B (2008) Effects of simulated light regimes on maturity and body composition of Antarctic krill, Euphausia superba. Mar Biol 154:315–324

    Article  Google Scholar 

  • Teschke M, Wendt S, Kawaguchi S, Kramer A, Meyer B (2011) A circadian clock in Antarctic krill: an endogenous timing system governs metabolic output rhythms in the euphausid species Euphausia superba. PLoS ONE 6(10):e26090

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Torres JJ, Aarset AV, Donnelly J, Hopkins TL, Lancraft TM, Ainley DG (1994) Proximate composition and overwintering strategies of Antarctic micronektonic crustacea. Mar Ecol Prog Ser 113:221–232

    Article  Google Scholar 

  • Vernet M, Kozlowski WA, Yarmey LR, Lowe AT, Ross RM, Quetin LB, Fritsen CH (2012) Primary production throughout austral fall, during a time of decreasing day length in the western Antarctic Peninsula. Mar Ecol Prog Ser 452:45–61

    Article  CAS  Google Scholar 

  • Vinagre AS, da Silva RSM (1992) Effects of starvation on the carbohydrate and lipid metabolism in crabs previously maintained on a high protein or carbohydrate-rich diet. Comp Biochem Physiol A 102:579–583

    Article  Google Scholar 

  • Virtue P, Nicol S, Nichols PD (1993) Changes in the digestive gland of Euphausia superba during short-term starvation: lipid class, fatty acid and sterol content and composition. Mar Biol 117:441–448

    CAS  Google Scholar 

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Acknowledgments

We are indebted to the crew of RV Aurora Australis for their great support and efforts during capture of krill and to Rob King for his professional support in the aquarium. We are grateful to C. Pape and D. Stübing for help with experiments, Toshihiro Yoshida for support in measuring oxygen uptake rates in krill, S. Spahic for expert support in sample analysis and P. Wencke for the excellent analytical work on the lipid biochemistry. This study was partially funded by the German Federal Ministry of Education and Research as part of the joint project “Seasonal population dynamics and physiological condition of the Antarctic krill—E. superba—in the Lazarev Sea” (BMBF 03F0400A) and supported by Australian Antarctic Science Program Project No.2337.

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    Authors and Affiliations

    1. Branch: Fisheries Management, Department of Agriculture, Forestry and Fisheries, Private Bag X2, 8012, Rogge Bay, Cape Town, Republic of South Africa

      Lutz Auerswald

    2. Department of Animal Sciences, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa

      Lutz Auerswald

    3. Scientific Division Biological Oceanography, Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570, Bremerhaven, Germany

      Bettina Meyer & Mathias Teschke

    4. BreMarE Bremen Marine Ecology, Marine Zoology, University of Bremen, P.O Box 330440, 28334, Bremen, Germany

      Wilhelm Hagen

    5. Australian Antarctic Division, 203 Channel Highway, Kingston, TAS, 7050, Australia

      So Kawaguchi

    6. Antarctic Climate and Ecosystems Cooperative Research Centre, Private Bag 80, Hobart, TAS, 7001, Australia

      So Kawaguchi

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    1. Lutz Auerswald
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    Correspondence to Lutz Auerswald.

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    Lutz Auerswald and Bettina Meyer have contributed equally to this work.

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    Auerswald, L., Meyer, B., Teschke, M. et al. Physiological response of adult Antarctic krill, Euphausia superba, to long-term starvation. Polar Biol 38, 763–780 (2015). https://doi.org/10.1007/s00300-014-1638-z

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    • DOI: https://doi.org/10.1007/s00300-014-1638-z

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