Insect winter ecology
Insect winter ecology describes the overwinter survival strategies of insects, which are in many respects more similar to those of plants than to many other animals, such as mammals and birds. Unlike those animals, which can generate their own heat internally, insects must rely on external sources to provide their heat. Thus, insects persisting in winter weather must tolerate freezing or rely on other mechanisms to avoid freezing. Loss of enzymatic function and eventual freezing due to low temperatures daily threatens the livelihood of these organisms during winter. Not surprisingly, insects have evolved a number of strategies to deal with the rigors of winter temperatures in places where they would otherwise not survive.
Two broad strategies for winter survival have evolved within Insecta as solutions to their inability to generate significant heat metabolically. Migration is a complete avoidance of the temperatures that pose a threat. An alternative to migration is weathering the cold temperatures present in its normal habitat. Insect cold tolerance is generally separated into two strategies, freeze avoidance and freeze tolerance.
Migration
Migration of insects differs from migration of birds. Bird migration is a two-way, round-trip movement of each individual, whereas this is not usually the case with insects. As a consequence of the short lifespan of insects, adult insects who have completed one leg of the trip may be replaced by a member of the next generation on the return voyage. As a result, invertebrate biologists redefine migration for this group of organisms in three parts:- A persistent, straight-line movement away from the natal area
- Distinctive pre- and post-movement behaviors
- Re-allocation of energy within the body associated with the movement
The monarch requires significant energy to make such a long flight, which is provided by fat reserves. When they reach their overwintering sites, they begin a period of lowered metabolic rate. Nectar from flowers procured at the overwintering site provides energy for the northward migration. To limit their energy use, monarchs congregate in large clusters in order to maintain a suitable temperature. This strategy, similar to huddling in small mammals, makes use of body heat from all the organisms and lowers heat loss.
Another common winter migrant insect, found in much of North America, South America, and the Caribbean, is the green darner. Migration patterns in this dragonfly species are much less studied than those of monarchs. Green darners leave their northern ranges in September and migrate south. Studies have noted a seasonal influx of green darners to southern Florida, which indicates migratory behavior. Little has been done with tracking of the green darner, and reasons for migration are not fully understood since there are both resident and migrant populations. The common cue for migration southward in this species is the onset of winter.
Cold tolerance
Insects that do not migrate from regions with the onset of colder temperatures must devise strategies to either tolerate or avoid lethal freezing of intracellular and extracellular body fluids. Insects that survive subfreezing temperatures are generally classified as freeze-avoidant or freeze-tolerant. The general strategy adopted by insects differs between the Northern Hemisphere and the Southern Hemisphere. In temperate regions of the northern hemisphere where cold temperatures are expected seasonally and are usually for long periods of time, the main strategy is freeze avoidance. In temperate regions of the southern hemisphere, where seasonal cold temperatures are not as extreme or long lasting, freeze tolerance is more common. However, in the Arctic, where freezing occurs seasonally, and for extended periods, freeze tolerance also predominates.Dangers of freezing
Intracellular ice formation usually causes cell death, even in freeze-tolerant species, due to physical stresses exerted as ice crystals expand. Ice formation in extracellular spaces increases the concentration of solutes in the extracellular fluid, resulting in the osmotic flow of water from intracellular spaces to extracellular spaces. Changes in solute concentration and dehydration can cause changes in enzyme activity and lead to the denaturation of proteins. If the temperature continues to decrease, the water that was drawn out of cells will also freeze, causing further cell shrinkage. Excessive cell shrinkage is dangerous because as ice forms outside the cell, the possible shapes that can be assumed by the cells are increasingly limited, causing damaging deformation. Finally, the expansion of ice within vessels and other spaces can cause physical damage to structures and tissues.Freeze avoidance
Freeze-avoidant insects cannot tolerate internal ice formation, so they avoid freezing by depressing the temperature at which their body fluids freeze. This is done through supercooling, the process by which a liquid cools below its freezing point without changing phase into a solid. In order for water to freeze, a nucleus must be present upon which an ice crystal can begin to grow. At low temperatures, nuclei may arise spontaneously from clusters of slow-moving water molecules. Alternatively, substances that facilitate the aggregation of water molecules can increase the probability that they will reach the critical size necessary for ice formation. If no source of nucleation is introduced, water can cool down to −48 °C without freezing. Therefore, when an insect maintains its body fluids in a supercooled state, there is the risk that spontaneous ice nucleation will occur. The temperature at which an insect spontaneously freezes is referred to as the supercooling point. For freeze-avoidant insects, the SCP is thought to be equivalent to the lower lethal temperature of the organism.The freezing process is usually initiated extracellularly in the gut, tissues, or hemolymph. In order to supercool to lower temperatures, freeze-avoidant insects will remove or inactivate ice-nucleating agents such as food particles, dust particles, and bacteria, found in the gut or intracellular compartments of these organisms. Removal of ice-nucleating material from the gut can be achieved by cessation in feeding, clearing the gut, and removing lipoprotein ice nucleators from the haemolymph.
Freezing can also be initiated by external contact with ice. Thus, some insects avoid freezing by selecting a dry hibernation site in which no ice nucleation from an external source can occur. Insects may also have a physical barrier such as a wax-coated cuticle that provides protection against external ice across the cuticle. The stage of development at which an insect over-winters varies across species, but can occur at any point of the life cycle. Some species of Collembola tolerate extreme cold by the shedding of the mid-gut during moulting.
In addition to physical preparations for winter, many insects also alter their biochemistry and metabolism. For example, some insects synthesize cryoprotectants such as polyols and sugars, which reduce the whole body SCP. Although polyols such as sorbitol, mannitol, and ethylene glycol can also be found, glycerol is by far the most common cryoprotectant and can be equivalent to ~20% of the total body mass. Glycerol is distributed uniformly throughout the head, the thorax, and the abdomen of insects, and is in equal concentration in intracellular and extracellular compartments. The depressive effect of glycerol on the supercooling point is thought to be due to the high viscosity of glycerol solutions at low temperatures. This would inhibit INA activity and SCPs would drop far below the environmental temperature. At colder temperatures, glycogen production is inhibited, and the breakdown of glycogen into glycerol is enhanced, resulting in the glycerol levels in freeze-avoidant insects reaching levels five times higher than those in freeze tolerant insects which do not need to cope with extended periods of cold temperatures.
Though not all freeze-avoidant insects produce polyols, all hibernating insects produce thermal hysteresis factors. For example, the haemolymph of the mealworm beetle Tenebrio molitor contains a family of such proteins. A seasonal photoperiodic timing mechanism is responsible for increasing the antifreeze protein levels with concentrations reaching their highest in the winter. In the pyrochroid beetle, Dendroides canadensis, a short photoperiod of 8 hours light and 16 hours of darkness, results in the highest levels of THFs, which corresponds with the shortening of daylight hours associated with winter. These antifreeze proteins are thought to stabilize SCPs by binding directly to the surface structures of the ice crystals themselves, diminishing crystal size and growth. Therefore, instead of acting to change the biochemistry of the bodily fluids as seen with cryoprotectants, THFs act directly with the ice crystals by adsorbing to the developing crystals to inhibit their growth and reduce the chance of lethal freezing occurring.
Freeze tolerance
Freeze tolerance in insects refers to the ability of some species to survive ice formation within their tissues. Insects that have evolved freeze-tolerance strategies manage to avoid tissue damage by controlling where, when, and to what extent ice forms. In contrast to freeze avoiding insects that are able to exist in cold conditions by supercooling, freeze-tolerant insects limit supercooling and initiate the freezing of their body fluids at relatively high temperatures. Some insects accomplish this through inoculative freezing, while others produce cryoprotectants to control the rate of ice formation. Freezing at higher temperatures is advantageous because the rate of ice formation is slower, allowing the insect time to adjust to the internal changes that result from ice formation.Most freeze-tolerant species restrict ice formation to extracellular spaces, as intracellular ice formation is usually lethal. Some species, however, are able to tolerate intracellular freezing. This was first discovered in the fat body cells of the goldenrod gall fly Eurosta solidaginis. The fat body is an insect tissue that is important for lipid, protein and carbohydrate metabolism. Although it is not certain why intracellular freezing is restricted to the fat body tissue in some insects, there is evidence that it may be due to the low water content within fat body cells.
Although freeze-avoidance strategies predominate in the insects, freeze tolerance has evolved at least six times within this group. Examples of freeze tolerant insects include: the woolly bear, Pyrrharctia isabella; the flightless midge, Belgica antarctica; the alpine tree weta, Hemideina maori; and the alpine cockroach, Celatoblatta quinquemaculata.
Freeze tolerance is more prevalent in insects from the Southern Hemisphere than it is in insects from the Northern Hemisphere. It has been suggested that this may be due to the Southern Hemisphere's greater climate variability, where insects must be able to survive sudden cold snaps yet take advantage of unseasonably warm weather as well. This is in contrast to the Northern Hemisphere, where predictable weather makes it more advantageous to overwinter after extensive seasonal cold hardening.