Hibernation: Poikilotherms

Abstract

Poikilothermic, or cold‐blooded animals face a risk of death due to cold or freezing over the winter and have evolved multiple strategies for survival. Some are unique options include migration by some butterfly and dragonfly species whereas honeybees heat their hive by shivering. Many animals are insulated from deep cold by hibernating underground or under water. For lung‐breathing turtles and frogs, under water hibernation requires novel adaptations: skin breathing by frogs and biochemical adaptations to survive without oxygen by turtles. Other poikilotherms manage to endure temperatures below 0°C. Many insects can prevent themselves from freezing with the use of antifreeze proteins and high concentrations of sugar alcohols that keep their body fluids liquid down to −40°C or lower. Other insects as well as some intertidal mollusks, and some frogs, turtles and lizards endure whole body freezing with adaptations that regulate ice formation in extracellular spaces, protect the intracellular environment and ensure the reactivation of heart beat, breathing and other vital functions after thawing.

Key Concepts:

  • To survive the winter, cold‐blooded animals need strategies that allow them to elude or endure exposures to environmental temperatures that are below the freezing point of their body fluids.

  • Some animals elude winter cold by migrating to warmer climates, others can dig down below the frost line or spend the winter in an aquatic environment that will not freeze.

  • Winter survival under water by lung‐breathing animals such as frogs and turtles often requires new strategies for acquiring oxygen, such as oxygen uptake across the skin by frogs or across the epithelial lining of the throat by some turtles.

  • Ice‐locked ponds and lakes often become oxygen‐depleted so many species have developed biochemical adaptations that allow them to survive without oxygen for weeks at a time.

  • Cold‐blooded animals that spend the winter on land have two choices for dealing with exposure to temperatures below 0°C: use antifreezes to prevent themselves from freezing or develop strategies to endure and regulate ice formation in their bodies.

  • The freeze avoidance strategy of survival used by many insects combines the production of special antifreeze proteins with the accumulation of high concentrations of glycerol or other polyhydric alcohols to keep body fluids liquid often to −40°C or lower.

  • Specialised antifreeze proteins are also used by many marine fish that live in polar regions or that come in contact with sea ice.

  • The freeze tolerance strategy of survival involves using sugars or polyhydric alcohols to protect the inside of cells while allowing specialised ice nucleating proteins to direct the formation of ice in body fluids cavities.

  • Freeze tolerant animals include many insects, some snails and barnacles that live in the intertidal zone and a few frog and reptile species that spend the winter on land; most can survive days or weeks frozen with 50–65% of their total body water frozen.

  • The molecular adaptations that allow animals to survive freezing have multiple potential applications for improving or developing methods for the cryopreservation of human cells, tissues and organs for use in medical transplantation.

Keywords: hibernation; freezing survival; cold hardiness; winter; dormancy; anoxia; antifreeze; cryoprotection; supercooling; migration

Figure 1.

(a) Schematic of the interaction of fish antifreeze protein (AFP) with ice. AFP binds to prism faces of ice crystals halting further growth in that plane. Growth continues in the basal plane but AFPs bind to new ice fronts forcing the crystal into a bipyramidal shape. (b) The bipyramidal ice crystal. (c) Structural model of the Type 1 AFP from flounders showing the α‐helical secondary structure. The protein shows repeating sequences of 11 amino acids (solid circles), 60% of which are alanine. Amino acids with hydrophilic side chains interact with ice; these are threonine (T), aspartic acid (D) and asparagine (N). Three other types of fish AFPs have different structures but bind to ice similarly. Adapted from Davies and Hew with permission from The Federation of American Societies for Experimental Biology.

Figure 2.

Freeze avoidance strategies of the goldenrod gall moth caterpillar, Epiblema scudderiana. (a) Depletion of the carbohydrate reserve, glycogen, supports the synthesis of high levels of glycerol that rise to over 2000 micromoles per gram wet mass in midwinter, or nearly 20% of the total body mass of the larva. (b) The supercooling point (SCP) of body fluids is strongly suppressed due to the combined action of seasonally synthesised AFPs and glycerol. These adaptations ensure that the SCP – which is the temperature at which the insect spontaneously freezes – always stays below the environmental mean minimum temperatures. (c) Gall moth caterpillar inside its gall; the caterpillar was removed from its silky cocoon (left) that protects it from coming in contact with any ice in the stem walls. (d) Two galls on a stem of goldenrod. Modified from Storey and Storey ; photos by Storey JM.

Figure 3.

The wood frog Rana sylvatica is the primary model animal used to study the mechanisms of vertebrate freeze tolerance, shown here in unfrozen (a) and frozen (b) states. Frogs winter on the forest floor and can endure several weeks of freezing at temperatures between −2 and −8°C with up to 65% of total body water frozen as extracellular ice. Ice nucleation on their skin triggers an immediate breakdown of glycogen in the frog's liver to produce glucose, which is then exported in high concentrations to all other organs to act as a cryoprotectant. Photos by Storey JM.

Figure 4.

Schematic showing how cells freeze. Ice formation begins in extracellular fluids stimulated by heterologous nucleators or, in freeze tolerant animals, by the actions of specific ice nucleating proteins (INPs). As ice grows, water is drawn out of cells to join the growing crystals whereas the concentrations of various solutes rise inside cells. In freeze tolerant animals, the production of high concentrations of glycerol (g) or other cryoprotectant prevents cell volume from shrinking below a critical minimum value whereas compounds such as trehalose and proline act as membrane protectants (MP) to stabilise membrane bilayer structure as cells shrink. Antifreeze proteins (AFPs) also help to modulate ice growth and inhibit recrystallisation during long‐term freezing. If frozen without protection, cell shrinkage is so severe that cell membranes collapse into an irreversible gel state and ice may penetrate into the cytoplasm, destroying subcellular architecture. Reproduced with permission from Storey and Storey .

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Further Reading

Heinrich B (2003) Winter World: The Ingenuity of Animal Survival. New York: Harper Collins.

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Roots C (2006) Hibernation. Westport, CT: Greenwood Publishing Group.

Storey KB (2004) Functional Metabolism: Regulation and Adaptation. Hoboken, NJ: Wiley‐Liss.

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Storey, Kenneth B, and Storey, Janet M(Sep 2011) Hibernation: Poikilotherms. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0003214.pub2]