Skip to main content
SpringerLink
Log in

Seasonal differences in citrate synthase and digestive enzyme activity in larval and postlarval antarctic krill, Euphausia superba

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Antarctic krill maintain large population sizes despite dramatic seasonal fluctuations in food availability, but the mechanisms for this are still debated. The aim of this study was to compare seasonal differences in enzyme activity and respiration rates of larval and postlarval krill to provide insights into their overwintering strategies. Respiration rates, activity of the metabolic enzyme citrate synthase (CS), and those of the digestive enzymes laminarinase and total proteinase were measured in austral summer west of the Antarctic Peninsula, and in autumn in the southwestern Lazarev Sea. The 100-fold difference in chlorophyll a concentrations between the two studies is representative of the classic transition from a summer bloom to sparse winter conditions. Correspondingly, adult krill showed reduced respiration rates and CS activity in autumn. However, their digestive enzyme activity was significantly higher, suggesting more efficient assimilation of food at low food levels. Similar-sized larvae showed no summer-autumn differences in respiration rates and enzyme activity, supporting suggestions that they need to feed and grow year-round. However, trends in enzymatic activity varied between the larval stages measured, implying ontogenetic changes in body structure and function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Atkinson A, Snÿder R (1997) Krill-copepod interactions at South Georgia, Antaretica I. Omnivory by Euphausia superba. Mar Ecol Prog Ser 160:63–76

    Article  Google Scholar 

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

    Google Scholar 

  • Båmstedt U, Gifford DJ, Irigoien X, Atkinson A, Roman M (2000) Feeding. In: Harris R, Wiebe P, Lenz J, Skjødal HR, Huntley M (eds) ICES zooplankton methodological manual. Academic Press, New York, pp 297–399

    Chapter  Google Scholar 

  • Barkley E (1940) Nahrung und Filterapparat des Walkrebschens Euphausia superba Dana. Z Fisch 1:65–156

    Google Scholar 

  • Buchholz F (1989) Moult cycle activities of chitinolytic enzymes in the integument and digestive tract of the Antarctic krill, Euphausia superba. Polar Biol 9:311–317

    Article  Google Scholar 

  • Buchholz F, Saborowski R (1996) A field study on the physiology of digestion in the Antaretic krill, Euphausia superba, with special regard to chitinolytic enzymes. J Plankton Res 18:895–906

    Article  CAS  Google Scholar 

  • Clarke A, Leakey RJG (1996) The seasonal cycle of phytoplankton, macronutrients and the microbial community in a nearshore Antarctic marine ecosystem. Limnol Oceanogr 41:1281–1294

    CAS  Google Scholar 

  • Clarke ME, Walsh PJ (1993) Effect of nutritional status on citrate synthase activity in Acartia tonsa and Temora longicornis. Limnol Oceanogr 38:414–418

    Article  CAS  Google Scholar 

  • Clarke ME, Calvi C, Domeier M, Edmonds M, Walsh PJ (1992) Effects of nutrition and temperature on metabolic enzyme activities in larval and juvenile red drum, Sciaenops ocellatus, and lane snapper Lutjanus synagris. Mar Biol 112:31–36

    Article  CAS  Google Scholar 

  • Cox JL, Willason SW (1981) Laminarinase induction in Calanus pacificus. Mar Biol 2:307–311

    CAS  Google Scholar 

  • Cripps GC, Atkinson A (2000) Fatty acid composition as an indicator of carnivory in Antarctic krill, Euphausia superba. Can J Fish Aquat Sci 57:31–37

    Article  CAS  Google Scholar 

  • Daly KL (1990) Overwintering development, growth, and feeding of larval Euphausia superba in the Antarctic marinal ice zone. Limnol Oceanogr 35:1564–1576

    Google Scholar 

  • Donachie SP, Saborowski R, Peters G, Buchholz F (1995) Bacterial digestive enzyme activity in the stomach and hepatopancreas of Meganyctiphanes norvegica (Sars M, 1857) J Exp Mar Biol Ecol 188:151–165

    Article  CAS  Google Scholar 

  • Donnelly J, Torres JJ, Hopkins TL, Lancraft TM (1990) Proximate composition of Antarctic mesopelagic fishes. Mar Biol 106:13–23

    Article  CAS  Google Scholar 

  • Fraser (1936) On the development and distribution of the young stages of krill Euphausia superba. Discov Rep 14:3–192

    Google Scholar 

  • Garrison DL, Sullivan CW, Ackley SF (1986) Sea ice microbial communities in Antarctica. BioScience 36:243–250

    Article  Google Scholar 

  • Hagen W (1988) On the significance of lipids in the Antarctic zooplankton. Rep Polar Res 49:1–129

    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 

  • Harris RP, Samain JF, Moal J, Martin-Jezequel V, Poulet SA (1986) Effects of algal diet on digestive activity in Calanus helgonadicus. Mar Biol 90:353

    Article  CAS  Google Scholar 

  • Hassett RP, Landry MR (1983) Effects of food-level acclimation on digestive enzyme activities and feeding behaviour of Calanus pacificus. Mar Biol 75:47–55

    Article  CAS  Google Scholar 

  • Haug A, Myklestad S (1973) Studies on the phytoplankton ecology of the Trondheimsfjord I. The chemical composition of phytoplankton populations. J Exp Mar Biol Ecol 11:15–26

    Article  CAS  Google Scholar 

  • Hernandez-Leon S, Portillo-Hahnefeld A, Almeida C, Becognee P, Moreno I (2001) Diel feeding behaviour of krill in the Gerlache Strait, Antarctica. Mar Ecol Prog Ser 223:235–242

    Article  Google Scholar 

  • Ikeda T (1981) Metabolic activity of larval stages of Antarctic krill. Antaret J US 16:161–162

    Google Scholar 

  • Ikeda T (1984) Sequences in metabolic rates and elemental composition (C, N, P) during the development of Euphausia superba Dana and estimated food requirements during its life span. J Crustac Biol 4 (spec vol 1):273–284

    Google Scholar 

  • Ikeda T (1985) Metabolic rates of pelagic marine zooplankton as a function of body mass and temperature. Mar Biol 85:1–11

    Article  Google Scholar 

  • Ikeda T, Dixon P (1984) The influence on feeding on the metabolic activity of Antarctic krill (Euphausia superba Dana). Polar Biol 3:1–9

    Article  Google Scholar 

  • Ikeda T, Torres JJ, Hernández-León S, Geiger SP (2000) Metabolism. In: Harris R, Wiebe P, Lenz J, Skjødal HR, Huntley M (eds) ICES zooplankton methodological manual. Academic Press, New York, 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 Crustac Biol 4:174–184

    Google Scholar 

  • Jones DA, Kumlu M, Le Vay L, Fletcher DJ (1997) The digestive physiology of herbivorous, omnivorous and carnivorous crustacean larvae: a review. Aquaculture 155:285–295

    Article  Google Scholar 

  • Kawagushi K, Ichikawa S, Matsuda O (1986) The overwintering strategy of Antarctic krill (Euphausia superba Dana) under the coastal fast ice off the Ongul Islands in Lutzow-Holm Bay Antarctica. (special issue) Mem Natl Inst Polar Res (Tokyo) 44:67–85

    Google Scholar 

  • Kils U (1983) Swimming and feeding of Antarctic krill, Euphausia superba — some outstanding energetic and dynamics — some unique morphological details. Ber Polarforsch (Sonderh) 4:130–155

    Google Scholar 

  • Marr JWS (1962) The natural history and geography of the Antarctic krill (Euphausia superba). Discov Rep 32:33–464

    Google Scholar 

  • Marschall H-P (1985a) Untersuchungen zur Funktionsmorphologie und Nahrungsaufnahme der Larven des Antarktischen Krills, Euphausia superba Dana. Ber Polarforsch 23:1–99

    Google Scholar 

  • Marschall H-P (1985b) Structural and functional analysis of the feeding appendages of krill larvae. In: Siegfried WR, Condy PR, Laws RM (eds) Antaretic nutrient cycles and food webs. Springer, Berlin Heidelberg New York, pp 346–354

    Google Scholar 

  • Mayzaud P, Conover RJ (1975) Influence of potential food supply on the activity of digestive enzymes of neritic zooplankton. In: Persone G, Jaspers E (eds) Proceedings of the 10th European Symposium of Marine Biology, vol 2. Universa Press, Wetteren, Belgium, pp 415–427

    Google Scholar 

  • Mayzaud P, Poulet SA (1978) The importance of the time factor in the response of zooplankton to varying concentrations of naturally occurring particulate matter. Limnol Oceanogr 23:1144–1154

    CAS  Google Scholar 

  • Mayzaud P, Farber-Lorda J, Corre MC (1985) Aspects of the nutritional metabolism of two Antaretic euphausiids: Euphausia superba and Thysonoessa macura. In: Siegfried WR, Condy PR, Laws RM (eds) Antaretic nutrient cycles and food webs. Springer, Berlin Heidelberg New York, pp 330–338

    Google Scholar 

  • McConville MJ, Ikeda T, Bacic A, Clarke AE (1986) Digestive carbohydrases from the hepatopancreas of two Antarctic euphausiid species (Euphausia superba and E. crystallorophias). Mar Biol 90:371–378

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Pakhomov EA, Perissinotto R, Froneman PW, Miller DGM (1997) Energetics and feeding dynamics of Euphausia superba in the South Georgia region during the summer of 1994. J Plankton Res 19:399–423

    Article  Google Scholar 

  • Peck LS, Whitehouse MJ (1992) An improved desorber design for use in couloximetry. J Exp Mar Biol Ecol 163:163–167

    Article  Google Scholar 

  • Pond DW, Priddle J, Sargent JR, Watkins JL (1995) Laboratory studies of assimilation and egestion of algal lipid by Antarctic krill — methods and initial results. J Exp Mar Biol Ecol 187:253–268

    Article  CAS  Google Scholar 

  • Power JH, Walsh PJ (1992) Metabolic scaling, buoyancy, and growth in larval Atlantic menhaden, Brevoortia tyrannus. Mar Biol 112:17–22

    Article  Google Scholar 

  • Price HJ, Boyd KR, Boyd CM (1988) Omnivorous feeding behaviour of the Antarctic krill Euphausia superba. Mar Biol 97:67–77

    Article  Google Scholar 

  • Quetin LB, Ross RM (1985) Feeding by Antarctic krill Euphausia superba: does size matter? In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin Heidelberg New York, pp 372–377

    Google Scholar 

  • Quetin LB, Ross RM (1991) Behavioural and physiological characteristics of the Antarctic krill, Euphausia superba. Am Zool 31:49–63

    Google Scholar 

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

    Google Scholar 

  • Quetin LB, Ross RM, Frazer TK, Habermann KL (1996) Factors affecting distribution and abundance of zooplankton, with an emphasis on Antarctic krill, Euphausia superba. Antarct Res Ser 70:357–371

    Google Scholar 

  • Ritz DA (2000) Is social aggregation in aquatic organisms a strategy to conserve energy? Can J Fish Aquat Sci 57:633–641

    Article  Google Scholar 

  • Ross RM, Quetin LB (1991) Ecological physiology of larval euphausiids, Euphausia superba (Euphausiaceae). Mem Queensl Mus 31:321–333

    Google Scholar 

  • Saborowski R, Buchholz F (1999) A laboratory study on digestive processes in the Antarctic krill, Euphausia superba, with special regard to chitinolytic enzymes. Polar Biol 21:295–304

    Article  Google Scholar 

  • Samain JF, Hernandorena A, Moal J, Daniel JY, Le Coz JR (1985) Amylase and trypsin activities during Artemia development on artificial ayenic media: effect of starvation and specific deletions. J Exp Mar Biol Ecol 86:255–270

    Article  CAS  Google Scholar 

  • Siegel V, Kalinowski J (1994) Krill demography and small scale processes: a review. In: El-Sayed S (ed) Southern Ocean ecology: the BIOMASS perspective. Cambridge University Press, Cambridge, pp 145–163

    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 

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

    Google Scholar 

  • Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis, 2nd edn. Bull Fish Res Bd Can 167:1–310

    Google Scholar 

  • Thuesen EV, Childress JJ (1993) Metabolic rates enzyme activities and chemical compositions of some deep-sea pelagic worms, particularly Nectonemertes mirabilis (Nemertea; Hoplonemertinea) and Poeobius meseres (Annelida, Polychaeta). Deep-Sea Res 1 Oceanogr Res Pap 40:937–951

    Article  CAS  Google Scholar 

  • Torres JJ, Somero, GN (1988) Metabolism, enzymic activities and cold adaption in Antarctic mesopelagic fishes. Mar Biol 98:169–180

    Article  CAS  Google Scholar 

  • Ullrich B, Storch V (1993) Development of the stomach in Euphausia superba Dana (Euphausiacea). J Crustac Biol 13:423–431

    Article  Google Scholar 

  • Ullrich B, Storch V, Marschall HP (1991) Microscopic anatomy, functional morphology, and ultrastructure of the stomach of Euphausia superba Dana (Crustacea, Euphausiacea). Polar Biol 11:203–211

    Article  Google Scholar 

  • Williamson DI (1982) Larval morphology and diversity In: Bliss DE (ed) The biology of Crustacea, vol 2. Embryology, morphology, and genetics. Academic Press, New York, pp 43–110

    Google Scholar 

  • Wolfe SH, Felgenhauer (1991) Mouthpart and foregut ontogeny in larval, postlarval, and juvenile lobster, Panulirus argus Latreille (Decapoda, Palinuridae). Zool Scripta 20:57–75

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pelagic Ecosystems, Alfred Wegener Institute for Polar and Marine Research, Handelshafen 12, 27570, Bremerhaven, Germany

    B. Meyer & U. Bathmann

  2. Biologische Anstalt Helgoland at the Alfred Wegener Institute, Marine Station, 27498, Helgoland, Germany

    R. Saborowski & F. Buchholz

  3. Natural Environment Research Council, British Antaretic Survey, High Cross, Madingley Road, CB3 0ET, Cambridge, UK

    A. Atkinson

Authors
  1. B. Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Saborowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Atkinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Buchholz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. U. Bathmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B. Meyer.

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Published online: 1 August 2002

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meyer, B., Saborowski, R., Atkinson, A. et al. Seasonal differences in citrate synthase and digestive enzyme activity in larval and postlarval antarctic krill, Euphausia superba . Marine Biology 141, 855–862 (2002). https://doi.org/10.1007/s00227-002-0877-7

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-002-0877-7

Keywords

Search

Navigation