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First published online May 30, 2008
Journal of Experimental Biology 211, 1903-1910 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.017558

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Slow desiccation improves dehydration tolerance and accumulation of compatible osmolytes in earthworm cocoons (Dendrobaena octaedra Savigny)

Christina R. Petersen^1,2, Martin Holmstrup^1,*, Anders Malmendal³, Mark Bayley² and Johannes Overgaard^1,2

¹ National Environmental Research Institute, University of Aarhus, Department of Terrestrial Ecology, Vejlsøvej 25, 8600 Silkeborg, Denmark
² Department of Zoophysiology, University of Aarhus, 8000 Aarhus C, Denmark
³ Center for Insoluble Protein Structures (inSPIN), Interdisciplinary Nanoscience Center (iNANO) and Department of Chemistry, University of Aarhus, 8000 Aarhus C, Denmark

^* Author for correspondence (e-mail: martin.holmstrup{at}dmu.dk)

Accepted 2 April 2008

The earthworm, Dendrobaena octaedra, is a common species in temperate and subarctic regions of the northern hemisphere. The egg capsules (`cocoons') of D. octaedra are deposited in the upper soil layers where they may be exposed to desiccation. Many previous studies on desiccation tolerance in soil invertebrates have examined acute exposure to harsh desiccating conditions, however, these animals are often more likely to be exposed to a gradually increasing drought stress. In the present study we slowly desiccated D. octaedra cocoons to simulate ecologically realistic drought conditions and the results clearly demonstrate that gradually dehydrated cocoons show an increased tolerance of extreme drought compared with acutely dehydrated cocoons. NMR spectroscopic analysis of compatible osmolytes revealed the presence of sorbitol, glucose, betaine, alanine and mannitol in dehydrated embryos. The superior drought survival of gradually desiccated embryos could partly be attributed to a higher accumulation of osmolytes (especially sorbitol). Thus, gradually and acutely desiccated embryos accumulated 2 mol l^–1 and 1 mol l^–1 total osmolytes, respectively. However, in addition to osmolyte accumulation, the gradually desiccated cocoons also tolerated a higher degree of water loss, demonstrating that gradually dehydrated D. octaedra cocoons are able to survive loss of 95% of the original water content. Although D. octaedra embryos can probably not be categorized as a truly anhydrobiotic organism we propose that they belong in a transition zone between the desiccation sensitive and the truly anhydrobiotic organisms. Clearly, these earthworm embryos share many physiological traits with anhydrobiotic organisms.

Key words: anhydrobiosis, betaine, dehydration, sorbitol, water loss