Skip to main content
SpringerLink
Log in

Coping with Ice: Freeze Avoidance in the Antarctic Silverfish (Pleuragramma antarctica) from Egg to Adult

  • Chapter
  • First Online:
Book cover The Antarctic Silverfish: a Keystone Species in a Changing Ecosystem

Part of the book series: Advances in Polar Ecology ((AVPE,volume 3))

Abstract

The Antarctic silverfish survives in a hostile environment that includes hatching into a zone laden with platelet ice. Embryonated eggs and hatchling larvae lack adequate levels of antifreeze to survive in this environment, but they are afforded physical protection against freezing by the presence of a resistant chorion (around the embryonated eggs) and a resistant external epithelium (around the larvae). Adult Antarctic silverfish also have low levels of antifreeze, but they are less likely to tolerate freezing conditions than their eggs or larvae because of damage to their external epithelium suffered during their lifetime allowing for ice entry. Like most other notothenioids, the Antarctic silverfish synthesises antifreeze glycoproteins (AFGPs), primarily in acinar cells of the exocrine pancreas. From here they are secreted directly into the digestive tract, ultimately dispersing throughout the body after uptake in the rectum and transfer into the blood circulatory system. Surprisingly, the Antarctic silverfish lacks the full range of AFGP isoforms (AFGP1-8), having instead a single dominant ~20 kDa form with some minor AFGP6 variants. The total serum AFGP concentration is relatively low, providing about 0.2 °C thermal hysteresis. Total serum hysteresis, however, is ~1.3 °C, the increase being provided by a novel antifreeze protein that behaves akin to the antifreeze potentiating protein (AFPP) described in other notothenioids. Nonetheless, this level of protection is below that required for survival in a freezing environment and thus adult Antarctic silverfish can only survive in locales free of ice crystals.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aarset AV, Jørgensen L (1988) Cold hardiness of the eggs of the plaice, Pleuronectes platessa. Polar Biol 9:95–99

    Article  Google Scholar 

  • Ahlgren JA, Cheng C-HC, Schrag JD et al (1988) Freezing avoidance and the distribution of antifreeze glycopeptides in body fluids and tissues of Antarctic fish. J Exp Biol 137:549–563

    CAS  Google Scholar 

  • Bilyk KT, Evans CW, DeVries AL (2012) Heat hardening in Antarctic notothenioid fishes. Polar Biol 35:1447–1451

    Article  Google Scholar 

  • Celik Y, Graham LA, Mok Y-F et al (2010) Superheating of ice crystals in antifreeze protein solutions. Proc Natl Acad Sci U S A 107:5423–5428

    Article  CAS  Google Scholar 

  • Celik Y, Drori R, Pertaya-Braun N et al (2013) Microfluidic experiments reveal that antifreeze proteins bound to ice crystals suffice to prevent their growth. Proc Natl Acad Sci U S A 110:1309–1314

    Article  CAS  Google Scholar 

  • Chen L, DeVries AL, Cheng C-HC (1997) Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc Natl Acad Sci U S A 94:3811–3816

    Article  CAS  Google Scholar 

  • Chen S, Li C, Yuan G, Xie F (2007) Anatomical and histological observation on the pancreas in adult zebrafish. Pancreas 34:120–125

    Article  Google Scholar 

  • Cheng C-HC (2003) Freezing avoidance in polar fishes. In: Gerday C (ed) Encyclopedia of life support systems (EOLSS) – theme 6.73 Extremophiles developed under the auspices of the UNESCO. Eolss Publishers, Oxford

    Google Scholar 

  • Cheng C-HC, Chen L (1999) Evolution of an antifreeze glycoprotein. Nature 40:443–444

    Article  Google Scholar 

  • Cheng C-HC, Cziko PA, Evans CW (2006) Nonhepatic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance. Proc Natl Acad Sci U S A 103:10491–10496

    Article  CAS  Google Scholar 

  • Cziko PA, Evans CW, Cheng C-HC et al (2006) Freezing resistance of antifreeze-deficient larval Antarctic fish. J Exp Biol 209:407–420

    Article  CAS  Google Scholar 

  • Cziko PA, DeVries AL, Evans CW et al (2014) Antifreeze protein-induced superheating of ice inside Antarctic notothenioid fishes inhibits melting during summer warming. Proc Natl Acad Sci U S A 111:14583–14588

    Article  CAS  Google Scholar 

  • Davenport J, Vahl O, Lonning S (1979) Cold resistance in the eggs of the capelin Mallotus villosus. J Mar Biol Assoc UK 59:443–454

    Article  Google Scholar 

  • Davies PL (2014) Ice-binding proteins: a remarkable diversity of structures for stopping (and starting) ice growth. TIBS 39:548–555

    CAS  Google Scholar 

  • Deng G, Andrews DW, Laursen RA (1997) Amino acid sequence of a new type of antifreeze protein, from the longhorn sculpin Myoxocephalus octodecimspinosis. FEBS Lett 402:17–20

    Article  CAS  Google Scholar 

  • DeVries AL (1971) Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172:1152–1155

    Article  CAS  Google Scholar 

  • DeVries AL (1988) The role of antifreeze glycopeptides and peptides in the freezing avoidance of Antarctic fishes. Comp Biochem Physiol B 90:611–621

    Article  Google Scholar 

  • DeVries AL, Cheng C-HC (2005) Antifreeze proteins and organismal freezing avoidance in polar fishes. In: Farrell AP, Steffensen JF (eds) Fish physiology, vol 22. Academic, San Diego, pp 155–201

    Google Scholar 

  • Duman JG (2014) An early classic study of freeze avoidance in marine fish. J Exp Biol 217:820–823

    Article  Google Scholar 

  • Evans RP, Fletcher GL (2004) Isolation and purification of antifreeze proteins from skin tissues of snailfish, cunner and sea raven. Biochim Biophys Acta 1700:209–217

    Article  CAS  Google Scholar 

  • Evans CW, Cziko P, Cheng C-HC et al (2005) Spawning behaviour and early development in the naked dragonfish Gymnodraco acuticeps. Antarct Sci 17:319–327

    Article  Google Scholar 

  • Evans CW, Gubala V, Nooney R et al (2011) How do Antarctic notothenioid fishes cope with internal ice? A novel function for antifreeze glycoproteins. Antarct Sci 23:57–64

    Article  Google Scholar 

  • Evans CW, Hellman L, Middleditch M et al (2012a) Synthesis and recycling of antifreeze glycoproteins in polar fishes. Antarct Sci 24:259–268

    Article  Google Scholar 

  • Evans CW, Williams DE, Vacchi M et al (2012b) Metabolic and behavioural adaptations during early development of the Antarctic silverfish, Pleuragramma antarcticum. Polar Biol 35:891–898

    Article  Google Scholar 

  • Field HA, Dong PD, Beis D et al (2003) Formation of the digestive system in zebrafish. II. Pancreas morphogenesis. Dev Biol 261:197–208

    Article  CAS  Google Scholar 

  • Fields LG, DeVries AL (2015) Variation in blood serum antifreeze activity of Antarctic Trematomus fishes across habitat temperature and depth. Comp Biochem Physiol A Mol Integr Physiol 185:43–50

    Article  CAS  Google Scholar 

  • Fletcher GL, Hew CL, Davies PL (2001) Antifreeze proteins of teleost fishes. Annu Rev Physiol 63:359–390

    Article  CAS  Google Scholar 

  • Gauthier SY, Scotter AJ, Lin FH et al (2008) A reevaluation of the role of type IV antifreeze protein. Cryobiology 57:292–296

    Article  CAS  Google Scholar 

  • Harvey B, Ashwood-Smith MJ (1982) Cryoprotectant penetration and supercooling in the eggs of salmonid fishes. Cryobiology 19:29–40

    Article  CAS  Google Scholar 

  • Hernandez-Blazquez FJ, Cunha da Silva JRM (1998) Absorption of macromolecular proteins by the rectal epithelium of the Antarctic fish Notothenia neglecta. Can J Zool 76:1247–1253

    Article  CAS  Google Scholar 

  • Hsiao KC, Cheng C-HC, Fernandes IE et al (1990) An antifreeze glycopeptide gene from the Antarctic cod Notothenia coriiceps neglecta encodes a polyprotein of high peptide copy number. Proc Natl Acad Sci U S A 87:9265–9269

    Article  CAS  Google Scholar 

  • Hudson AP, DeVries AL et al (1979) Antifreeze glycoprotein biosynthesis in Antarctic fishes. Comp Biochem Physiol B 62:179–183

    Article  Google Scholar 

  • Jin Y (2003) Freezing avoidance of Antarctic fishes: the role of a novel antifreeze potentiating protein and the antifreeze glycoproteins. PhD dissertation, University of Illinois at Urbana-Champaign

    Google Scholar 

  • Knight CA, DeVries AL (1989) Melting inhibition and superheating of ice by an antifreeze glycopeptide. Science 245:505–507

    Article  CAS  Google Scholar 

  • Lee JK, Kim YJ, Park KS et al (2011) Molecular and comparative analyses of type IV antifreeze proteins (AFPIVs) from two Antarctic fishes, Pleuragramma antarcticum and Notothenia coriiceps. Comp Biochem Physiol B 159(4):197–205

    Article  Google Scholar 

  • Mazur P (1970) Cryobiology: the freezing of biological systems. Science 168:939–949

    Article  CAS  Google Scholar 

  • McGuinness MJM, Williams JM, Langhorne PJ et al (2009) Frazil deposition under growing sea ice. J Geophys Res 114:C07014

    Article  Google Scholar 

  • Peck L (2015) DeVries: the art of not freezing fish. J Exp Biol 218:2146–2147

    Article  Google Scholar 

  • Peltier R, Brimble MA, Wojnar JM et al (2010) Synthesis and antifreeze activity of fish antifreeze glycoproteins and their analogues. Chem Sci 1:538–551

    Article  CAS  Google Scholar 

  • Praebel K, Hunt B, Hunt L et al (2009) The presence and quantification of splenic ice in the McMurdo Sound notothenioid fish, Pagothenia borchgrevinki (Boulenger, 1902). Comp Biochem Physiol 154A:564–569

    Article  CAS  Google Scholar 

  • Raymond JA (1992) Glycerol is a colligative antifreeze in some northern fishes. J Exp Zool 262:347–352

    Article  CAS  Google Scholar 

  • Raymond JA, DeVries AL (1977) Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc Natl Acad Sci U S A 76:2589–2593

    Article  Google Scholar 

  • Robinson NJ, Williams MJM, Stevens CL et al (2014) Evolution of a supercooled ice shelf water plume with an actively growing sub-ice platelet matrix. J Geophys Res Oceans 119:3425–3446

    Article  Google Scholar 

  • Terblanche JS, Hoffmann AA, Mitchel KA et al (2011) Ecologically relevant measures of tolerance to potentially lethal temperatures. J Exp Biol 214:3713–3725

    Article  Google Scholar 

  • Thompson SN (2003) Trehalose – the insect ‘blood’ sugar. Adv Insect Physiol 31:205–285

    Article  CAS  Google Scholar 

  • Tiso N, Moro E, Argenton F (2009) Zebrafish pancreas development. Mol Cell Endocrinol 312:24–30

    Article  CAS  Google Scholar 

  • Vacchi M, Bottaro M, DeVries AL et al (2012) A nursery area for the Antarctic silverfish Pleuragramma antarcticum at Terra Nova Bay (Ross Sea): first estimate of distribution and abundance of eggs and larvae under the seasonal sea-ice. Polar Biol 35:1573–1585

    Article  Google Scholar 

  • Valerio PF, Goddard SV, Kao MH et al (1992a) Survival of northern Atlantic cod (Gadus morhua) eggs and larvae when exposed to ice and low temperature. Can J Fish Aquat Sci 49:2588–2595

    Article  Google Scholar 

  • Valerio PF, Kao MH, Fletcher GL (1992b) Fish skin: an effective barrier to ice crystal propagation. J Exp Biol 164:135–151

    Article  Google Scholar 

  • Wan H, Korzh S, Li Z et al (2006) Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastase A gene promoter. Exp Cell Res 312:1526–1539

    Article  CAS  Google Scholar 

  • Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:98–411

    Google Scholar 

  • Wöhrmann APA (1996) Antifreeze glycopeptides and peptides in Antarctic fish species from the Weddell Sea and the Lazarev Sea. Mar Ecol Prog Ser 130:47–59

    Article  Google Scholar 

  • Wöhrmann APA (1997) Freezing resistance in Antarctic and Arctic fishes: its relation to mode of life, ecology and evolution. Cybium 21:423–442

    Google Scholar 

  • Wöhrmann 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 151:205–218

    Article  Google Scholar 

  • Xiao Q, Xia JH, Zhang XJ et al (2014) Type-IV antifreeze proteins are essential for epiboly and convergence in gastrulation of zebrafish embryos. Int J Biol Sci 10(7):715–732

    Article  CAS  Google Scholar 

  • Yang S-H, Wojnar JM, Harris PWR et al (2013) Chemical synthesis of a masked analogue of the fish antifreeze potentiating protein (AFPP). Org Biomol Chem 11:4935–4942

    Article  CAS  Google Scholar 

  • Zambonino Infante JL, Cahu CL (2001) Ontogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Physiol C 130:477–487

    CAS  Google Scholar 

Download references

Acknowledgements

Supported in part by a grant from Office of Polar Programs, NSF to ALD. We thank colleagues at Scott Base, McMurdo Station and Stazione Mario Zucchelli for field assistance, and the respective national Antarctic programmes for logistic support. We are grateful to Vivian Ward for her assistance with the graphics, and Liyana Nouxman for her contribution to the microscopy.

This manuscript is dedicated to the memory of John A Macdonald, our friend and colleague who was a respected and much liked long-term member of the Antarctic scientific community.

Author information

Authors and Affiliations

  1. School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

    Clive W. Evans

  2. Department of Animal Biology, University of Illinois at Urbana-Champaign, 524 Burrill Hall, 407 S. Goodwin, Urbana, IL, 61801, USA

    Arthur L. DeVries

Authors
  1. Clive W. Evans
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arthur L. DeVries
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Clive W. Evans .

Editor information

Editors and Affiliations

  1. Institute of Marine Sciences (ISMAR) - CNR, Genoa, Italy

    Marino Vacchi

  2. Department of Earth, Environment and Life Sciences (DISTAV), University of Genoa, Genoa, Italy

    Eva Pisano

  3. Institute of Marine Sciences (ISMAR) - CNR, Genoa, Italy

    Laura Ghigliotti

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Evans, C.W., DeVries, A.L. (2017). Coping with Ice: Freeze Avoidance in the Antarctic Silverfish (Pleuragramma antarctica) from Egg to Adult. In: Vacchi, M., Pisano, E., Ghigliotti, L. (eds) The Antarctic Silverfish: a Keystone Species in a Changing Ecosystem. Advances in Polar Ecology, vol 3. Springer, Cham. https://doi.org/10.1007/978-3-319-55893-6_2

Download citation

Publish with us

Policies and ethics

Search

Navigation