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First published online January 19, 2006
Journal of Experimental Biology 209, 407-420 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02008

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Freezing resistance of antifreeze-deficient larval Antarctic fish

Paul A. Cziko¹, Clive W. Evans², Chi-Hing C. Cheng^1,* and Arthur L. DeVries¹

¹ Department of Animal Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA
² Molecular Genetics and Development, School of Biological Sciences, University of Auckland, Auckland, New Zealand

^* Author for correspondence (e-mail: c-cheng{at}uiuc.edu)

Accepted 22 November 2005

Antarctic notothenioids, along with many other polar marine fishes, have evolved biological antifreeze proteins (AFPs) to survive in their icy environments. The larvae of Antarctic notothenioid fish hatch into the same frigid environment inhabited by the adults, suggesting that they must also be protected by sufficient AFPs, but this has never been verified. We have determined the contribution of AFPs to the freezing resistance of the larvae of three species: Gymnodraco acuticeps, Pagothenia borchgrevinki and Pleuragramma antarcticum. Of the three, only P. borchgrevinki larvae are protected by high, adult levels of AFPs. Hatchling G. acuticeps and P. antarcticum have drastically inadequate AFP concentrations to avoid freezing at the ambient seawater temperature (-1.91°C). We raised G. acuticeps larvae and measured the AFP levels in their blood for 5 months post hatching. Larval serum freezing point was -1.34±0.04°C at the time of hatch; it began to decrease only after 30 days post hatch (d.p.h.), and finally reached the adult value (-2.61±0.03°C) by 147 d.p.h. Additionally, AFP concentrations in their intestinal fluids were very low at hatching, and did not increase with age throughout a sampling period of 84 d.p.h.

Surviving in a freezing environment without adequate AFP protection suggests that other mechanisms of larval freezing resistance exist. Accordingly, we found that G. acuticeps hatchlings survived to -3.6±0.1°C while in contact with external ice, but only survived to -1.5±0.0°C when ice was artificially introduced into their tissues. P. antarcticum larvae were similarly resistant to organismal freezing. The gills of all three species were found to be underdeveloped at the time of hatch, minimizing the risk of ice introduction through these delicate structures. Thus, an intact integument, underdeveloped gill structures and other physical barriers to ice propagation may contribute significantly to the freezing resistance and survival of these larval fishes in the icy conditions of the Southern Ocean.

Key words: Notothenioidei, Bathydraconidae, Nototheniidae, antifreeze glycoprotein, antifreeze potentiating protein, development, gills, mitochondrial NADH dehydrogenase subunit 2, temperature logging

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This article has been cited by other articles:

				Z. Chen, C.-H. C. Cheng, J. Zhang, L. Cao, L. Chen, L. Zhou, Y. Jin, H. Ye, C. Deng, Z. Dai, et al. Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish PNAS, September 2, 2008; 105(35): 12944 - 12949. [Abstract] [Full Text] [PDF]

				C.-H. C. Cheng, P. A. Cziko, and C. W. Evans Nonhepatic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance PNAS, July 5, 2006; 103(27): 10491 - 10496. [Abstract] [Full Text] [PDF]