Biologists have long been interested in the occurrence of insects at the extremes of the Earth, in surprising diversity and sometimes in large numbers. Holometabolous insects are abundant in refugial sites within 3° of the North Pole, although fewer, notably a chironomid midge and some penguin and seal lice, are found on the Antarctic proper. Freezing, high elevations, including glaciers, sustain resident insects, such as the Himalayan Diamesa glacier midge (Diptera: Chironomidae), which sets a record for cold activity, being active at an air temperature of —16°C. Snowfields also support seasonally cold-active insects such as grylloblattids, and Chionea (Diptera: Tipulidae) and Boreus (Mecoptera), the snow “fleas”. Low-temperature environments pose physiological problems that resemble dehydration in the reduction of available water, but clearly also include the need to avoid freezing of body fluids. Expansion and ice crystal formation typically kill mammalian cells and tissues, but perhaps some insect cells can tolerate freezing. Insects may possess one or several of a suite of mechanisms — collectively termed cryoprotection — that allows survival of cold extremes. These mechanisms may apply in any lifehistory stage, from resistant eggs to adults. Although they form a continuum, the following categories can aid understanding.
Freeze-tolerant insects include some of the most cold- hardy species, mainly occurring in Arctic, sub-Arctic, and Antarctic locations that experience the most extreme winter temperatures (e.g. —40 to —80°C). Protection is provided by seasonal production of ice- nucleating agents (INA) under the induction of falling temperatures and prior to onset of severe cold. These proteins, lipoproteins, and/or endogenous crystalline substances such as urates, act as sites where (safe) freezing is encouraged outside cells, such as in the hemolymph, gut, or Malpighian tubules. Controlled and gentle extracellular ice formation acts also to gradually dehydrate cell contents, in which state freezing is avoided. In addition, substances such as glycerol and/or related polyols, and sugars including sorbitol and trehalose, allow supercooling (remaining liquid at subzero temperature without ice formation) and also protect tissues and cells prior to full INA activation and after freezing. Antifreeze proteins may also be produced; these fulfill some of the same protective roles, especially during freezing conditions in fall and during the spring thaw, outside the core deep-winter freeze. Onset of internal freezing often requires body contact with external ice to trigger ice nucleation, and may take place with little or no internal supercooling. Freeze tolerance does not guarantee survival, which depends not only on the actual minimum temperature experienced but also upon acclimation before cold onset, the rapidity of onset of extreme cold, and perhaps also the range and fluctuation in temperatures experienced during thawing. In the well-studied galling tephritid fly Eurosta solidaginis, all these mechanisms have been demonstrated, plus tolerance of cell freezing, at least in fat body cells.
Freeze avoidance describes both a survival strategy and a species’ physiological ability to survive low temperatures without internal freezing. In this definition, insects that avoid freezing by supercooling can survive extended periods in the supercooled state and show high mortality below the supercooling point, but little above it, and are freeze avoiders. Mechanisms for encouraging supercooling include evacuation of the digestive system to remove the promoters of ice nucleation, plus pre-winter synthesis of polyols and anti- freeze agents. In these insects cold hardiness (potential to survive cold) can be calculated readily by comparison of the supercooling point (below which death occurs) and the lowest temperature the insect experiences. Freeze avoidance has been studied in the autumnal moth, Epirrita autumnata, and goldenrod gall moth, Epiblema scudderiana.
Chill-tolerant species occur mainly from temperate areas polewards, where insects survive frequent encounters with subzero temperatures. This category contains species with extensive supercooling ability (see above) and cold tolerance, but is distinguished from these by mortality that is dependent on duration of cold exposure and low temperature (above the supercooling point), i.e. the longer and the colder the freezing spell, the more deaths are attributable to freezing-induced cellular and tissue damage. A notable ecological grouping that demonstrates high chill tolerance are species that survive extreme cold (lower than supercooling point) by relying on snow cover, which provides “milder” conditions where chill tolerance permits survival. Examples of studied chill-tolerant species include the beech weevil, Rhynchaenus fagi, in Britain, and the bertha armyworm, Mamestra configurata, in Canada.
Chill-susceptible species lack cold hardiness, and although they may supercool, death is rapid on exposure to subzero temperatures. Such temperate insects tend to vary in summer abundances according to the severity of the preceding winter. Thus, several studied European pest aphids (Myzus persicae, Sitobion avenae, and Rhopalosiphum padi) can supercool to —24°C (adults) or —27°C (nymphs) yet show high mortality when held at subzero temperatures for just a minute or two. Eggs show much greater cold hardiness than nymphs or adults. As overwintering eggs are produced only by sexual (holocyclic) species or clones, aphids with this life cycle predominate at increasingly high latitudes in comparison with those in which over- wintering is in a nymphal or adult stage (anholocyclic species or clones).
Opportunistic survival is observed in insects living in stable, warm climates in which cold hardiness is little developed. Even though supercooling is possible, in species that lack avoidance of cold through diapause or quiescence (section 6.5), mortality occurs when an irreversible lower threshold for metabolism is reached. Survival of predictable or sporadic cold episodes for these species depends upon exploitation of favorable sites, for example by migration (section 6.7) or by local opportunistic selection of appropriate microhabitats.
Clearly, low-temperature tolerance is acquired convergently, with a range of different mechanisms and chemistries involved. A unifying feature may be that the mechanisms for cryoprotection are rather similar to those shown for avoidance of dehydration which may be preadaptive for cold tolerance. Although each of the above categories contains a few unrelated species, amongst the terrestrial bembidiine Carabidae (Coleoptera) the Arctic and sub-Arctic regions contain a radiation of cold-tolerant species. A preadaptation to aptery (wing loss) has been suggested for these beetles, as it is too cold to warm flight muscles. Nonetheless, the summer Arctic is plagued by actively flying, biting dipterans that warm themselves by their resting orientation towards the sun.