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First published online August 14, 2009
Journal of Experimental Biology 212, 2803-2811 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.029413

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Cyclomorphosis in Tardigrada: adaptation to environmental constraints

Kenneth Agerlin Halberg¹, Dennis Persson^1,2, Hans Ramløv³, Peter Westh³, Reinhardt Møbjerg Kristensen² and Nadja Møbjerg^1,*

¹ Department of Biology, University of Copenhagen, August Krogh Building, Universitetsparken 13, DK-2100 Copenhagen Ø, Denmark
² Natural History Museum of Denmark, Zoological Museum, Invertebrate Department, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark
³ Department of Nature, Systems and Models, University of Roskilde, Universitetsvej 1, DK-4000 Roskilde, Denmark

^* Author for correspondence (e-mail: nmobjerg{at}bio.ku.dk)

Accepted 9 June 2009

Tardigrades exhibit a remarkable resilience against environmental extremes. In the present study, we investigate mechanisms of survival and physiological adaptations associated with sub-zero temperatures and severe osmotic stress in two commonly found cyclomorphic stages of the marine eutardigrade Halobiotus crispae. Our results show that only animals in the so-called pseudosimplex 1 stage are freeze tolerant. In pseudosimplex 1, as well as active-stage animals kept at a salinity of 20 ppt, ice formation proceeds rapidly at a crystallization temperature of around –20°C, revealing extensive supercooling in both stages, while excluding the presence of physiologically relevant ice-nucleating agents. Experiments on osmotic stress tolerance show that the active stage tolerates the largest range of salinities. Changes in body volume and hemolymph osmolality of active-stage specimens (350–500 µm) were measured following salinity transfers from 20 ppt. Hemolymph osmolality at 20 ppt was approximately 950 mOsm kg^–1. Exposure to hypo-osmotic stress in 2 and 10 ppt caused (1) rapid swelling followed by a regulatory volume decrease, with body volume reaching control levels after 48 h and (2) decrease in hemolymph osmolality followed by a stabilization at significantly lower osmolalities. Exposure to hyperosmotic stress in 40 ppt caused (1) rapid volume reduction, followed by a regulatory increase, but with a new steady-state after 24 h below control values and (2) significant increase in hemolymph osmolality. At any investigated external salinity, active-stage H. crispae hyper-regulate, indicating a high water turnover and excretion of dilute urine. This is likely a general feature of eutardigrades.

Key words: cyclomorphosis, environmental stress, freeze tolerance, Halobiotus crispae, invertebrate, osmoregulation, tardigrade, volume regulation

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