Dealing With Environmental Extremes

The most obvious environmental variables that confront an insect are seasonal fluctuations in temperature and humidity. The extremes of temperatures and humidities experienced by insects in their natural environments span the range of conditions encountered by terrestrial organisms, with only the suite of deep oceanic hydrothermic vent taxa encountering higher temperatures. For reasons of human interest in cryobiology (revivable preservation) the responses to extremes of cold and desiccation have been better studied than those to high temperatures alone.

The options available for avoidance of the extremes are behavioral avoidance, such as by burrowing into soil of a more equable temperature, migration (section 6.7), diapause (section 6.5), and in situ tolerance/ survival in a very altered physiological condition, the topic of the following sections.

6.6.1 Cold

Biologists have long been interested in the occurrence of insects at the extremes of the Earth, in surprising diversity and sometimes in large numbers. Holometa-bolous insects are abundant in refugial sites within 3° of the North Pole, although fewer, notably a chirono-mid 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: Chirono-midae), 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 gryl-loblattids, 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 life-history stage, from resistant eggs to adults. Although they form a continuum, the following categories can aid understanding.

Freeze tolerance

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

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 nucle-ation, plus pre-winter synthesis of polyols and antifreeze 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 tolerance

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 susceptibility

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 —2 7°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 overwintering is in a nymphal or adult stage (anholocyclic species or clones).

Opportunistic survival

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 con-vergently, 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.

6.6.2 Heat

The hottest inhabited places on Earth occur in the ocean, where suboceanic thermal vents support a unique assemblage of organisms based on thermo-philous bacteria, and insects are absent. In contrast, in a terrestrial equivalent, vents in thermally active areas support a few specialist insects. The hottest waters in thermal springs of Yellowstone National Park are too hot to touch, but by selection of slightly cooler microhabitats amongst the cyanobacteria/blue-green algal mats, a brine fly, Ephydra bruesi (Ephydridae), can survive at 43°C. At least some other species of ephydrids, stratiomyiids, and chironomid larvae (all Diptera) tolerate nearly 50°C in Iceland, New Zealand, South America, and perhaps other sites where volcanism provides hot-water springs. The other aquatic temperature-tolerant taxa are found principally amongst the Odonata and Coleoptera.

High temperatures tend to kill cells by denaturing proteins, altering membrane and enzyme structures and properties, and by loss of water (dehydration). Inherently, the stability of non-covalent bonds that determine the complex structure of proteins determines the upper limits, but below this threshold there are many different but interrelated temperature-dependent biochemical reactions. Exactly how insects tolerant of high temperature cope biochemically is little known. Acclimation, in which a gradual exposure to increasing (or decreasing) temperatures takes place, certainly provides a greater disposition to survival at extreme temperatures compared with instantaneous exposure. When comparisons of effects of temperature are made, acclimation conditioning should be considered.

Options of dealing with high air temperatures include behaviors such as use of a burrow during the hottest times. This activity takes advantage of the buffering of soils, including desert sands, against temperature extremes so that near-stable temperatures occur within a few centimeters of the fluctuations of the exposed surface. Overwintering pupation of temperate insects frequently takes place in a burrow made by a late-instar larva, and in hot, arid areas night-active insects such as predatory carabid beetles may pass the extremes of the day in burrows. Arid-zone ants, including Saharan Cataglyphis, Australian Melophorus, and Namibian Ocymyrmex, show several behavioral features to maximize their ability to use some of the hottest places on Earth. Long legs hold the body in cooler air above the substrate, they can run as fast as 1m s—11, and are good navigators to allow rapid return to the burrow. Tolerance of high temperature is an advantage to Cataglyphis because they scavenge upon insects that have died from heat stress. However, Cataglyphis bombycina suffers predation from a lizard that also has a high temperature tolerance, and predator avoidance restricts the above-ground activity of Cataglyphis to a very narrow temperature band, between that at which the lizard ceases activity and its own upper lethal thermal threshold. Cataglyphis minimizes exposure to high temperatures using the strategies outlined above, and adds thermal respite activity - climbing and pausing on grass stems above the desert substrate, which may exceed 46°C. Physiologically, Cataglyphis may be amongst the most thermally tolerant land animals because they can accumulate high levels of "heat-shock proteins" in advance of their departure to forage from their (cool) burrow to the ambient external heat. The few minutes duration of the foraging frenzy is too short for synthesis of these protective proteins after exposure to the heat.

The proteins once termed "heat-shock proteins" (abbreviated as "hsp") may be best termed stress-induced proteins when involved in temperature-related activities, as at least some of the suite can be induced also by desiccation and cold. Their function at higher temperatures appears to be to act as molecular chaper-ones assisting in protein folding. In cold conditions, protein folding is not the problem, but rather it is loss of membrane fluidity, which can be restored by fatty acid changes and by denaturing of membrane phospholipids, perhaps also under some control of stress proteins.

The most remarkable specialization involves a larval chironomid midge, Polypedilum vanderplanki, which lives in West Africa on granite outcrops in temporary pools, such as those that form in depressions made by native people when grinding grain. The larvae do not form cocoons when the pools dry, but their bodies lose water until they are almost completely dehydrated. In this condition of cryptobiosis (alive but with all metabolism ceased), the larvae can tolerate temperature extremes, including artificially imposed temperatures in dry air from more than 100°C down to -2 7°C. On wetting, the larvae revive rapidly, feed and continue development until the onset of another cycle of desiccation or until pupation and emergence.

6.6.3 Aridity

In terrestrial environments, temperature and humidity are intimately linked, and responses to high temperatures are inseparable from concomitant water stress. Although free water may be unavailable in the arid tropics for long periods, many insects are active year-round in places such as the Namib Desert, an essentially rain-free desert in southwestern Africa. This desert has provided a research environment for the study of water relations in arid-zone insects ever since the discovery of "fog basking" amongst some tenebrionid beetles. The cold oceanic current that abuts the hot Namib Desert produces daily fog that sweeps inland. This provides a source of aerial moisture that can be precipitated onto the bodies of beetles that present a head-down stance on the slip face of sand dunes, facing the fog-laden wind. The precipitated moisture then runs to the mouth of the beetle. Such atmospheric water gathering is just one from a range of insect behaviors and morphologies that allow survival under these stressful conditions. Two different strategies exemplified by different beetles can be compared and contrasted: detritivorous tenebrionids and predaceous carabids, both of which have many aridity-tolerant species.

The greatest water loss by most insects occurs via evaporation from the cuticle, with lesser amounts lost through respiratory gas exchange at the spiracles and through excretion. Some arid-zone beetles have reduced their water loss 100-fold by one or more strategies including extreme reduction in evaporative water loss through the cuticle (section 2.1), reduction in spiracular water loss, reduction in metabolism, and extreme reduction of excretory loss. In the studied aridzone species of tenebrionids and carabids, cuticular water permeability is reduced to almost zero such that water loss is virtually a function of metabolic rate alone - i.e. loss is by the respiratory pathway, predominantly related to variation in the local humidity around the spiracles. Enclosure of the spiracles in a humid sub-elytral space is an important mechanism for reduction of such losses. Observation of unusually low levels of sodium in the hemolymph of studied tenebrionids compared with levels in arid-zone carabids (and most other insects) implies reduced sodium pump activity, reduced sodium gradient across cell membranes, a con-comitantly inferred reduction in metabolic rate, and reduced respiratory water loss. Uric acid precipitation when water is reabsorbed from the rectum allows the excretion of virtually dry urine (section 3.7.2), which, with retention of free amino acids, minimizes loss of everything except the nitrogenous wastes. All these mechanisms allow the survival of a tenebrionid beetle in an arid environment with seasonal food and water shortage. In contrast, desert carabids include species that maintain a high sodium pump activity and sodium gradient across cell membranes, implying a high metabolic rate. They also excrete more dilute urine, and appear less able to conserve free amino acids. Behav-iorally, carabids are active predators, needing a high metabolic rate for pursuit, which would incur greater rates of water loss. This may be compensated for by the higher water content of their prey, compared with the desiccated detritus that forms the tenebrionid diet.

To test if these distinctions are different "adaptive" strategies, or if tenebrionids differ more generally from carabids in their physiology, irrespective of any arid tolerance, will require wider sampling of taxa, and some appropriate tests to determine whether the observed physiological differences are correlated with taxo-nomic relationships (i.e. are preadaptive for life in low-humidity environments) or ecology of the species. Such tests have not been undertaken.

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