Polar Biology

, Volume 35, Issue 6, pp 891–898 | Cite as

Metabolic and behavioural adaptations during early development of the Antarctic silverfish, Pleuragramma antarcticum

  • Clive W. Evans
  • David E. Williams
  • Marino Vacchi
  • Margaret A. Brimble
  • Arthur L. DeVries
Original Paper


The Antarctic silverfish Pleuragramma antarcticum is a keystone species in the Ross Sea ecosystem, providing one of the major links between lower and higher trophic levels. Despite the importance of this species, surprisingly little is known of its early development and behaviour. Here, we determine the metabolic capacity of Pleuragramma embryonated eggs and larvae and make comparisons with developing stages of another notothenioid, the naked dragonfish Gymnodraco acuticeps. We also show that although large numbers of embryonated eggs of Pleuragramma are found floating among the platelet ice of Terra Nova Bay, they are able to sink prior to hatching in late spring, likely reducing the risk of exposure to the potentially lethal, ice-laden surface environment. Applying Stoke’s law, we determine the change in density required for embryonated eggs to sink at the measured rate and then consider possible mechanisms by which this might occur. Significantly, newly hatched larvae are positively gravitactic and negatively phototactic, such that their swimming behaviour also directs them away from the risk of freezing in the icy surface waters. Measurement of the acute thermal tolerance shows that Pleuragramma larvae have, on average, a sustainable swimming performance breadth of about 17°C, which is significantly greater than that of other adult notothenioids. Although it lacks significant antifreeze capacity in its early developmental stages, Pleuragramma has other attributes that may ensure survival over a wider range of environmental temperatures than other more stenothermal Antarctic notothenioids. How it might adapt to prolonged environmental change arising from phenomena such as global warming, however, requires further investigation.


Pleuragramma Developmental descent Metabolism Behaviour Phototaxis Gravitaxis Thermal tolerance Ross Sea ecosystem 



This work was supported by the National Science Foundation, Office of Polar Programs (#02-31006) and the Human Frontier Science Programme (RGP003/2009-C). The field activity at Stazione Mario Zucchelli was supported by the Italian Antarctic Project PNRA as part of the project ECOFISH (2004/8.04). We thank Paul Cziko, Eva Pisano and Lauren Fields for their input, our colleagues at Stazione Mario Zucchelli and Scott Base for their help and companionship in the field, and our referees (JT Eastman and DG Ainley) for their helpful comments.

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. Bilyk KT, DeVries AL (2011) Heat tolerance and its plasticity in Antarctic fishes. Comp Biochem Physiol A 158:382–390CrossRefGoogle Scholar
  2. Blaxter JHS, Ehrlich KF (1974) Changes in behaviour during starvation of herring and plaice larvae. In: Blaxter JHS (ed) The early life history of fish. Springer, New York, pp 575–588CrossRefGoogle Scholar
  3. Calow P (1977) Conversion efficiencies in heterotrophic organisms. Biol Rev 52:385–409CrossRefGoogle Scholar
  4. Coombs SH (1981) A density-gradient column for determining the specific gravity of fish eggs, with particular reference to eggs of the mackerel Scomber scombrus. Mar Biol 63:101–106CrossRefGoogle Scholar
  5. Coombs SH, Boyra G, Rueda LD, Uriarte A, Santos M, Conway DVP, Halliday NC (2004) Buoyancy measurements and vertical distribution of eggs of sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus). Mar Biol 145:959–970CrossRefGoogle Scholar
  6. Cziko PA, Evans CW, Cheng C-HC, DeVries AL (2006) Freezing resistance of antifreeze-deficient larval Antarctic fish. J Exp Biol 209:407–420PubMedCrossRefGoogle Scholar
  7. DeVries AL (1988) The role of glycopeptide and peptide antifreeze in the freezing avoidance of Antarctic fishes. Comp Biochem Physiol 90B:611–621Google Scholar
  8. DeVries AL, Eastman JT (1978) Lipid sac as a buoyancy adaptation in an Antarctic fish. Nature 271:352–353CrossRefGoogle Scholar
  9. DeWitt HH (1970) The character of the midwater fish fauna of the Ross Sea, Antarctica. In: Holdgate MW (ed) Antarctic ecology, vol 1. Academic Press, London, pp 305–315Google Scholar
  10. Eastman JT, DeVries AL (1981) Buoyancy adaptations in a swim-bladderless Antarctic fish. J Morphol 167:91–102CrossRefGoogle Scholar
  11. Eastman JT, DeVries AL (1982) Buoyancy studies of notothenioid fishes in McMurdo Sound, Antarctica. Copeia 1982:385–393CrossRefGoogle Scholar
  12. Evans CW, Pace L, Cziko PA, Marsh AG, Cheng C-HC, DeVries AL (2006) Metabolic energy utilization during development of Antarctic naked dragonfish (Gymnodraco acuticeps). Polar Biol 29:519–525CrossRefGoogle Scholar
  13. Evans CW, Gubala V, Nooney R, Williams DE, Brimble MA, DeVries AL (2011) How do Antarctic notothenioid fishes cope with internal ice? A novel function for antifreeze glycoproteins. Antarct Sci 23:57–64CrossRefGoogle Scholar
  14. Grillitsch S, Medgyesy N, Schwerte T, Pelster B (2005) The influence of environmental P O2 on haemoglobin oxygen saturation in developing zebrafish Danio rerio. J Exp Biol 298:309–316CrossRefGoogle Scholar
  15. Jacobs SS, Giulivi CH, Mele PA (2002) Freshening of the Ross Sea during the late 20th century. Science 297:386–389PubMedCrossRefGoogle Scholar
  16. La Mesa M, Eastman JT, Vacchi M (2004) The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review. Polar Biol 27:321–338CrossRefGoogle Scholar
  17. Needham J (1931) Chemical embryology, vol 2. CUP, Cambridge, pp 946–986Google Scholar
  18. Paladino FV, Spotila JR, Schubauer JP, Kowalski KT (1980) The critical thermal maximum—a technique used to elucidate physiological stress and adaptation in fishes. Rev Can Biol 39:115–122Google Scholar
  19. Pelster B, Burggren WW (1996) Disruption of haemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebrafish (Danio rerio). Circ Res 79:358–362PubMedGoogle Scholar
  20. Peltier R, Brimble MA, Wojnar JM, Williams DE, Evans CW, DeVries AL (2010) Synthesis and antifreeze activity of fish antifreeze glycoproteins and their analogues. Chem Sci 1:538–551CrossRefGoogle Scholar
  21. Quillin ML, Matthews BW (2000) Accurate calculation of the density of proteins. Acta Crystallogr D Biol Crystallogr 56:791–794PubMedCrossRefGoogle Scholar
  22. Ramsing N, Gundersen J (2011) Seawater and gases. Unisense. Accessed 1 Nov 2011
  23. Sclafani M, Stirling G, Leggett WC (2000) Osmotic condition, buoyancy change and mortality in larval cod Gadus morhua. A bioassay for assessing near term mortality. Mar Ecol Prog Ser 193:157–166CrossRefGoogle Scholar
  24. Smith WO, Ainley DG, Cattaneo-Vietti R, Hofmann EE (2011) The Ross Sea continental shelf: regional biogeochemical cycles, trophic interactions, and potential future changes. In: Rogers AD, Murphy EJ, Johnston, NM, Clarke A (eds) Antarctica: an extreme environment in a changing world, Chapter 7. Wiley, LondonGoogle Scholar
  25. Somero GN, DeVries AL (1967) Temperature tolerance of some Antarctic fishes. Science 156:257–258PubMedCrossRefGoogle Scholar
  26. Vacchi M, La Mesa M, Dali M, Macdonald J (2004) Early life stages in the life cycle of Antarctic silverfish Pleuragramma antarcticum in Terra Nova Bay, Ross Sea. Antarct Sci 16:299–305CrossRefGoogle Scholar
  27. Wilson RS, Kuchel LJ, Franklin CE, Davison W (2002) Turning up the heat on subzero fish: thermal dependence of sustained swimming in an Antarctic notothenioid. J Therm Biol 27:381–386CrossRefGoogle Scholar
  28. Wohrmann APA, Hagen W, Kunzmann A (1997) Adaptations of the Antarctic silverfish Pleuragramma antarcticum (Pisces: Nototheniidae) to pelagic life in High Antarctic waters. Mar Ecol Prog Ser 151:205–218CrossRefGoogle Scholar
  29. Yin MC, Blaxter JHS (1987) Temperature, salinity tolerance, and buoyancy during early development and starvation of Clyde and North Sea herring, cod and flounder larvae. J Exp Mar Biol Ecol 107:279–290CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Clive W. Evans
    • 1
  • David E. Williams
    • 2
  • Marino Vacchi
    • 3
  • Margaret A. Brimble
    • 2
  • Arthur L. DeVries
    • 4
  1. 1.School of Biological Sciences, University of AucklandAucklandNew Zealand
  2. 2.School of Chemical Sciences, University of AucklandAucklandNew Zealand
  3. 3.ISPRA, c/o Museo Nazionale dell’Antartide, Università di GenovaGenoaItaly
  4. 4.Department of Animal BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

Personalised recommendations