Insect Freeze Avoidance

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By Geof Gaiser
Freeze avoidance is clearly the basal characteristic of insects, in contrast to freeze tolerance, an evolved set of traits.  Avoidance is characteristic of cold continental habitats of the Northern Hemisphere, allowing insects to survive very low temperatures for long periods of time, and also to avoid desiccation.  These responses tend to be strongly seasonal, and insects in these habitats are only capable of maintaining their avoidance strategies for the overwintering period in their microenvironment. Strategies of freeze avoidance are seen in the larvae of the goldenrod gall moth, Epiblema scudderiana,eggs of the Autumnal moth, Epirrita autumna,  many other insects, and the arachnids – spiders, mites and ticks. Some super cooling points can be as low as -35 to -40ᵒC. 

Ref.   B.J.Sinclair et al “Climatic variability and the evolution of insect freeze tolerance”, Biological Reviews, 78:181-195 (2003)

The larvae of the goldenrod gall moth mentioned above, are freeze intolerant. Falling temperatures stimulate cryoprotectant formation, with larvae exposed to 1ᵒC per day decrease in temperature show a major increase in the rate of glycerol synthesis. When temperatures fall below 5ᵒC this rises to its highest rate of synthesis. Abrupt re-warming of larvae from -18ᵒC up to 23ᵒC in mid-November stimulates a rapid loss (conversion) of glycerol.  Re-warming of cold-adapted larvae late in November results in only a small rise in the Super Cooling Point (and did not break diapauses), but rewarming in February resulted in a 19ᵒC rise in Super Cooling Point in just 4 days, followed by rapid pupation. This appears to be related to seasonal or photoperiod recognition.

Ref. Mary Jane Kelleher et al. Journal of Insect Physiology, V33, Issue 8, Pages 581-586

Challenges to Freeze Avoidance survival are presented by modern climate change with its increased variability in weather patterns including freezing episode occurrence and severity.
Physiological responses are needed to deal with:
o   Increased temperature extremes (levels)
o   Increased rates of temperature change
o   Increased frequency of freeze/thaw transitions
o   Increased unpredictability of freezing and thawing events
o   The variability of the weather effects on the surrounding microhabitat

Ref. B.J.Sinclair et al “Insects at Low Temperatures: An Ecological Perspective” in Trends in Ecology and Evolution V18(5):257-262, May 2003
               
Freeze Avoidance usually involves an evacuation of the digestive system.  Some populations experience freeze mortality of most individuals, but because they are present in many microenvironments, a few survive to repopulate the habitat in spring.  Other species, such as the Autumnal Moth Epirrita autumnata that defoliates birch trees in northern Scandinavia, are frozen to death in all stages of life, except the eggs, which can survive down to nearly -36ᵒC.
               
Ref.  J.S. Bale “Insect Cold Hardiness: A Matter of Life and Death”  European Journal of Entomology 369-382  (1996)

The Stag Beetle Ceruchus piceus, is freeze sensitive. It cannot survive internal freezing. It produces very low quantities of anti-freezing compounds. It survives to -25ᵒC by removing lipoproteins from its gut and hemolymph, which would nucleate ice crystals if present.

Ref. Charles Burks Comparative Physiology B: Biochemical, Systematic and Environmental Physiology 156:707-716 (1986)

Micro-climate survival in the Canadian prairies is shown by the bertha armyworm Mamestra configurata pupae that over-winter 2-15 cm deep in soil, and super-cool there to -20ᵒC. Soil temperature cools to 0ᵒC for 5-6 months every year. Approximately once per 4 years soil temperature may descend to -15ᵒC allowing for survival.

Most aphids overwinter as eggs for species survival when their other life cycle forms die off. Adult aphids of three species survive to -24ᵒC but their eggs survive to -27ᵒC. their nymphs are more cold tolerant than the adults. With an adaptation that is similar to some plants that can reproduce asexually when under environmental stress, asexually produced aphids have better freeze survivability than those that developed sexually.

Aphids wintering in the same microenvironment as their food source, plant leaves, survive freezing temperatures better (even when their food source is frozen) than the aphids isolated from plant material.

Ref. J.S. Bale  as above


Insect Freeze Tolerance

Several metabolic traits evolved that biochemically protect freeze damage.
Three molecular mechanisms:
1.       Glycogen to Polyol (antifreeze) conversion
2.       Reversible protein phosphorylation (which makes the protein more resistant to steric denaturing from freezing)
3.       This phosphorylation also depresses the enzyme activity that reconverts polyols back to glycogen

Ref.  Charles Burks “Biochemical Adaptation for Cold Hardiness in Insects” Philosophical Transactions of the Royal Society of London B 326 (1237):635-654 (1990)

In freeze tolerant insects, ice nucleating agents are synthesized in autumn and early winter (not removed as a survival strategy in freeze avoiding insects). These promote safe, extracellular freezing down to -5 to -10ᵒC in the hemolymph and in other extra-cellular parts of the body.

Antifreeze proteins are anabolized that inhibit re-crystallization during frequent intermittent freeze/thaw cycles in spring and fall.

Ref. J.S. Bale in Eurpean Journal Entomology as above.

Once frozen, Freeze Tolerant Insects can be cooled to -50ᵒC, then thaw, recover and show normal development, reproduction and behavior.  More insect species are freeze tolerant that are freeze intolerant (avoidant).

Ref. J.S.Bale “Classes of Insect Cold Hardiness” in Functional Ecology V7 No6, Dec 1993 pp 751-753



 

Examples of Freeze Tolerant Insects


Lepidoptera – Sesamia Inferen (Lepidoptera: Noctuidae) the pink rice-stem borer is a major rice pest in Asia. It survives freezing by forming accumulations of simple sugars and polyols.




American cockroach, Periplaneta americana

Blattodea –cockroaches and termites. The smallest varieties of each exhibit the highest freeze tolerance. The larger species are tropical. Some cockroaches have survived -122ᵒC by making a polyol out of glycerol.


Hoverfly adults and pupa

Diptera – The hoverfly Syrphus ribesii larvae have 70% survival at -35ᵒC accomplished with ice nucleating activity.









Orthoptera – New Zealand alpine weta Hemideina maori Hutton (Orthoptera:Stenopelmatidae)
                Survival below its super cooling point by making unidentified non-ionic non-carbohydrate compounds






Coleoptera – Bark Beetles  (Coleoptera:Scolytidae)  The most cold adapted type migrate to the forest floor in winter, such as Ips pinis and Ips grandicollis.
 

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