Physiology of cold hardiness in earthworms

Physiological, biochemical and behavioral mechanisms involved in the winter survival of earthworms and earthworm cocoons are reviewed. Overwintering strategies of cold hardy invertebrates are commonly divided into two groups. In freeze-avoiding animals, ice formation in the tissues is lethal and winter survival is dependent on prolonged and extensive supercooling. Freeze-tolerant animals tolerate extracellular freezing up to a certain fraction of the body water. Hatched earthworms belong to the first group, having a behaviorally-based strategy, escaping frost in the soil by migration. The cold hardiness mechanism of earthworm cocoons is based on a protective dehydration of cocoons occurring when cocoons are exposed to subzero temperatures in a frozen environment. Due to the lower vapour pressure of ice compared to supercooled water at a given temperature, water evaporates from the cocoon surface and condenses onto ice in the surroundings. Dehydration of cocoons continues until vapour pressure equilibrium between cocoon fluids and surrounding ice is attained. At equilibrium the cocoons cannot freeze since the melting point of cocoon fluids equals ambient temperature. Because the melting point of cocoon fluids is high, -0.2 to -0.4 degrees C, the cocoons lose substantial amounts of water, even at mild freezing exposures. As a response to dehydration the embryos of the cocoons accumulate a polyol, probably sorbitol, which may prevent deleterious effects of the extensive water loss coupled with vapour equilibration. Since dehydration is a key event when earthworm cocoons are exposed to low temperatures it is likely that tolerance to drought is important for cold survival. Substantial support for this hypothesis has been found in Dendrobaena octaedra which is far more tolerant to drought and cold than other investigated species. It is suggested that the described ''protective dehydration mechanism'' of cold hardiness should be considered in cold hardiness studies of other soil animals with high cuticular evaporation rates.