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Freeze or dehydrate: only two options for the survival of subzero temperatures in the arctic enchytraeid Fridericia ratzeli

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Abstract

Hygrophilic soil animals, like enchytraeids, overwintering in frozen soil are unlikely to base their cold tolerance on supercooling of body fluids. It seems more likely that they will either freeze due to inoculative freezing, or dehydrate and adjust their body fluid melting point to ambient temperature as has been shown for earthworm cocoons and Collembola. In the present study we tested this hypothesis by exposing field-collected adult Fridericia ratzeli from Disko, West Greenland, to freezing temperatures under various moisture regimes. When cooled at −1 °C min−1 under dry conditions F. ratzeli had a mean temperature of crystallisation (T c) of −5.8 °C. However, when exposed to temperatures above standard T c for 22 h, at −4 °C, most individuals (90%, n= 30) remained unfrozen. Slow cooling from −1 °C to −6 °C in vials where the air was in equilibrium with the vapour pressure of ice resulted in freezing in about 65% of the individuals. These individuals maintained a normal body water content of 2.7–3.0 mg mg−1 dry weight and had body fluid melting points of about −0.5 °C with little or no change due to freezing. About 35% of the individuals dehydrated drastically to below 1.1 mg mg−1 dry weight at −6 °C, and consequently had lowered their body fluid melting point to ca. −6 °C at this time. Survival was high in both frozen and dehydrated animals at −6 °C, about 60%. Approximately 25% of the animals (both frozen and dehydrated individuals) had elevated glucose concentrations, but the mean glucose concentration was not increased to any great extent in any group due to cold exposure. The desiccating potential of ice was simulated using aqueous NaCl solutions at 0 °C. Water loss and survival in this experiment were in good agreement with results from freezing experiments. The influence of soil moisture on survival and tendency to dehydrate was also evaluated. However, soil moisture ranging between 0.74 g g−1 and 1.15 g g−1 dry soil did not result in any significant differences in survival or frequency of dehydrated animals even though the apparent wetness and structure of the soil was clearly different in these moisture contents.

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Abbreviations

DW :

dry weight

FW :

fresh weight

MP :

melting point

RH:

relative humidity

Tc:

crystallisation temperatures

WC :

water content

References

  • Bauer R (2002) Survival of frost and drought conditions in the soil by enchytraeids (Annelida; Oligochaeta) in Arctic, subalpine and temperate areas. Eur J Soil Biol 38:251–254

    Article  Google Scholar 

  • Bauer R, Kiem R, Pfeffer M (1998) Winter survival and cold hardiness in Stercutus niveus (Oligochaeta, Enchytraeidae). Appl Soil Ecol 9:87–92

    Article  Google Scholar 

  • Birkemoe T (1995) Population dynamics of Enchytraeidae at the arctic tundra at Spitzbergen, Svalbard. Newsletter on Enchytraeidae 4:45–52

    Google Scholar 

  • Birkemoe T, Coulson SJ, Sømme L (2000) Life cycles and population dynamics of enchytraeids (Oligochaeta) from the High Arctic. Can J Zool 78:2079–2086

    Article  Google Scholar 

  • Block W (1984) A comparative study of invertebrate supercooling at Signy Island, Maritime Antarctic. Br Antarct Surv Bull 64:67–76

    Google Scholar 

  • Block W, Bauer R (2000) DSC studies of freezing in terrestrial enchytraeids (Annelida: Oligochaeta). Cryo-Lett 21:99–106

    Google Scholar 

  • Costanzo JP, Moore JB, Lee RE Jr, Kaufman PE, Wyman JA (1997) Influence of soil hydric parameters on the winter cold hardiness of a burrowing beetle, Leptinotarsa decemlineata (Say). J Comp Physiol B 167:169–176

    Article  Google Scholar 

  • Costanzo JP, Bayuk JM, Lee RE Jr (1999) Inoculative freezing by environmental ice nuclei in the freeze-tolerant wood frog, Rana sylvatica. J Exp Zool 284:7–14

    Article  CAS  PubMed  Google Scholar 

  • Coulson S, Birkemoe T (2000) Long-term cold tolerance in Arctic invertebrates: recovery after 4 years at below −20  °C. Can J Zool 78:2055–2058

    Article  Google Scholar 

  • Coulson S, Hodkinson I, Strathdee A, Block W, Webb N, Bale J, Worland M (1995) Thermal environments of arctic soil organisms during winter. Arctic Alpine Res 27:364–370

    Google Scholar 

  • Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599

    Google Scholar 

  • Damgaard C, Weiner J (2000) Describing inequality in plant size or fecundity. Ecology 81:1139–1142

    Google Scholar 

  • Didden WAM (1993) Ecology of terrestrial Enchytraeidae—review. Pedobiologia 37:2–29

    Google Scholar 

  • Dozsa-Farkas K (1973) Some preliminary data on the frost tolerance of enchytraeidae. Opusc Zool Budapest 11:95–97

    Google Scholar 

  • Edwards J (1986) How small ectotherms thrive in the cold without really trying. Cryo Letters 6:388–390

    Google Scholar 

  • Holmstrup M (2002) Strategies for cold and drought tolerance in permeable soil invertebrates. Doctor's dissertation (DSc), National Environmental Research Institute, Silkeborg, Denmark.

  • Holmstrup M, Sjursen H (2001) Freeze-induced glucose accumulation in the enchytraeid, Fridericia ratzeli, from Greenland. Cryo Letters 22:273–276

    CAS  PubMed  Google Scholar 

  • Holmstrup M, Sømme L (1998) Dehydration and cold hardiness in the Arctic collembolan Onychiurus arcticus Tullberg 1876. J Comp Physiol B 168:197–203

    Article  Google Scholar 

  • Holmstrup M, Westh P (1994) Dehydration of earthworm cocoons exposed to cold: a novel cold hardiness mechanism. J Comp Physiol B 164:312–315

    Google Scholar 

  • Holmstrup M, Costanzo J, Lee RE (1999) Cryoprotective and osmotic responses to cold acclimation and freezing in freeze-tolerant and freeze-intolerant earthworms. J Comp Physiol B 169:207–214

    Article  Google Scholar 

  • Holmstrup M, Sjursen H, Ravn H, Bayley M (2001) Dehydration tolerance and water vapour absorption in two species of soil-dwelling Collembola by accumulation of sugars and polyols. Funct Ecol 15:647–653

    Article  Google Scholar 

  • Holmstrup M, Bayley M, Ramløv H (2002) Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable arctic invertebrates. PNAS USA 99:5716–5720

    Article  CAS  PubMed  Google Scholar 

  • Klungland T (1981) Abundance fluctuations of Enchytraeids in two high-mountain localities in Southern Norway. Pedobiologia 22:112–140

    Google Scholar 

  • Miller RD (1980) Freezing phenomena in soils. In: Hillel D (ed) Applications of soil physics. Academic Press, New York, pp 254–299

  • Nurminen M (1967) Ecology of enchytraeids (Oligochaeta) in Finnish coniferous forest soil. Ann Zool Fennici 4:147–157

    Google Scholar 

  • Nurminen M (1970) Records of enchytraeidae (Oligochaeta) from the west coast of Greenland. Ann Zool Fennici 7:199–209

    Google Scholar 

  • Oglesby L (1969) Inorganic components and metabolism; ionic and osmotic regulation: Annelida, Sipuncula and Echiura. In: Florkin M, Scheer BT (eds) Chemical zoology, Vol IV: Annelida, Echiura and Sipuncula. Academic Press, New York, pp 211–310

  • Petersen H, Luxton M (1982) A comparative analysis of soil fauna populations and their role in decomposition. Oikos 39:287–388

    Google Scholar 

  • Prentø P (1987) Blood sugar, sugar metabolism and related enzymes in the earthworm, Lumbricus terrestris L. Comp Biochem Physiol B 86:333–341

    Article  Google Scholar 

  • Ramløv H (2000) Aspects of natural cold tolerance in ectothermic animals. Hum Reprod 15:26–46

    PubMed  Google Scholar 

  • Rasmussen L, Holmstrup M (2002) Geographic variation of freeze-tolerance in the earthworm Dendrobaena octaedra. J Comp Physiol B 172:691–698

    Article  CAS  PubMed  Google Scholar 

  • Salt W (1963) Delayed inoculative freezing of insects. Can Entomol 95:1190–1202

    Google Scholar 

  • Storey KB (1997) Organic solutes in freezing tolerance. Comp Biochem Physiol A 117:319–326

    Google Scholar 

  • Sømme L, Birkemoe T (1997) Cold tolerance and dehydration in Enchytraeidae from Svalbard. J Comp Physiol B 167:264–269

    Article  Google Scholar 

  • Swift MJ, Andren O, Brussaard L, Briones M, Couteaux MM, Ekschmitt K, Kjøller A, Loiseau P, Smith P (1998) Global change, soil biodiversity, and nitrogen cycling in terrestrial ecosystems—three case studies. Global Change Biol 4:729–743

    Article  Google Scholar 

  • Wharton DA, Goodall G, Marshall CJ (2003) Freezing survival and cryoprotective dehydration as cold tolerance mechanisms in the Antarctic nematode Panagrolaimus davidi. J Exp Biol 206:215–221

    Article  PubMed  Google Scholar 

  • Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65:799–831

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Arctic Station, Godhavn, Disko, is thanked for accommodation and laboratory facilities. In particular we thank Bente Jessen Graae for giving us the best working conditions during our field work. Bent Christensen is thanked for taxonomic guidance, and Christian Damgaard for statistical assistance. We also thank Tobias Wang and Hans Ramløv for comments on earlier drafts of the manuscript. Nordic Arctic Research Programme and The Danish Natural Science Research Council granted financial support for this study. The experiments described in this paper comply with Danish legislation.

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Correspondence to M. Holmstrup.

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Communicated by I.D. Hume

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Pedersen, P.G., Holmstrup, M. Freeze or dehydrate: only two options for the survival of subzero temperatures in the arctic enchytraeid Fridericia ratzeli . J Comp Physiol B 173, 601–609 (2003). https://doi.org/10.1007/s00360-003-0370-8

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