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First published online August 17, 2006
Journal of Experimental Biology 209, 3469-3475 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02387
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Freezing or supercooling: how does an aquatic subterranean crustacean survive exposures at subzero temperatures?

Julien Issartel1,*, Yann Voituron2, Valentina Odagescu3, Anne Baudot3, Geneviève Guillot4, Jean-Pierre Ruaud4, David Renault5, Philippe Vernon5 and Frédéric Hervant1

1 Ecologie des Hydrosystèmes Fluviaux, UMR CNRS 5023, Université Claude Bernard Lyon 1, 69622 Villeurbanne cedex, France
2 Laboratoire Souterrain de Moulis (CNRS), 09200 Moulis, France
3 Centre de Recherches sur les Très Basses Températures, CNRS, BP 166, 38042, Grenoble cedex 9, France
4 Unité de Recherche en Résonance Magnétique Médicale, UMR 8081 CNRS-Université Paris-Sud 91405 Orsay, France
5 Ecosystèmes - Biodiversité - Evolution, UMR CNRS 6553, Université Rennes 1, 35042 Rennes cedex, France

* Author for correspondence (e-mail: julien.issartel{at}univ-lyon1.fr)

Accepted 15 June 2006

Crystallization temperature (Tc), resistance to inoculative freezing (IF), ice contents, bound water, protein and glycogen body contents were measured in the aquatic subterranean crustacean Niphargus rhenorhodanensis and in the morphologically close surface-dwelling aquatic crustacean Gammarus fossarum, both acclimated at 12°C, 3°C and -2°C. Cold acclimation induced an increase in the Tc values in both species but no survival was observed after thawing. However, after inoculation at high sub-zero temperatures, cold-acclimated N. rhenorhodanensis survived whereas all others, including the 3°C and -2°C acclimated G. fossarum died. In its aquatic environment, N. rhenorhodanensis is likely to encounter inoculative freezing before reaching the Tc and IF tolerance appears as a highly adaptive trait in this species. Bound water and glycogen were found to increase in the 3°C and -2°C acclimated N. rhenorhodanensis, whereas no variation was observed in G. fossarum. Considering the hydrophilic properties of glycogen, such a rise may be correlated with the increased bound water measured in cold-acclimated N. rhenorhodanensis, and may be linked to the survival of this species when it was inoculated. The ecological significance of the survival of the aquatic subterranean crustacean to inoculative freezing is paradoxical, as temperature is currently highly buffered in its habitat. However, we assume that past geographical distribution and resulting life history traits of N. rhenorhodanensis are key parameters in the current cold-hardiness of the species.

Key words: crustaceans, subterranean, epigean, freezing tolerance, bound water, crystallisation temperature, inoculative freezing, ice content, cold acclimation, glycogen






© The Company of Biologists Ltd 2006